July 2005
Volume 46, Issue 7
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Visual Neuroscience  |   July 2005
Differential Behavior of Simple and Complex Cells in Visual Cortex during a Brief IOP Elevation
Author Affiliations
  • Xin Chen
    From the Vision Research Laboratory, Center for Brain Science Research, Department of Ophthalmology and Vision Science and State Key Laboratory of Medical Neurobiology, School of Life Sciences, Fudan University, Shanghai, China; and the
  • Zhiyin Liang
    From the Vision Research Laboratory, Center for Brain Science Research, Department of Ophthalmology and Vision Science and State Key Laboratory of Medical Neurobiology, School of Life Sciences, Fudan University, Shanghai, China; and the
  • Wei Shen
    From the Vision Research Laboratory, Center for Brain Science Research, Department of Ophthalmology and Vision Science and State Key Laboratory of Medical Neurobiology, School of Life Sciences, Fudan University, Shanghai, China; and the
  • Tiande Shou
    From the Vision Research Laboratory, Center for Brain Science Research, Department of Ophthalmology and Vision Science and State Key Laboratory of Medical Neurobiology, School of Life Sciences, Fudan University, Shanghai, China; and the
    Laboratory of Visual Information Processing, Chinese Academy of Sciences, Beijing, China.
Investigative Ophthalmology & Visual Science July 2005, Vol.46, 2611-2619. doi:10.1167/iovs.04-0874
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      Xin Chen, Zhiyin Liang, Wei Shen, Tiande Shou; Differential Behavior of Simple and Complex Cells in Visual Cortex during a Brief IOP Elevation. Invest. Ophthalmol. Vis. Sci. 2005;46(7):2611-2619. doi: 10.1167/iovs.04-0874.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

purpose. To study and compare responses of different types of cortical neurons in the primary visual cortex in cats to grating stimuli before and during brief elevation of intraocular pressure (IOP).

methods. Single-unit electrophysiological recordings were performed in anesthetized and paralyzed cats. The IOP was elevated by injecting saline into the anterior chamber of the cat’s eyes through a syringe needle. The IOP was elevated to a level at which the retinal perfusion pressure (arterial pressure minus IOP) was maintained at approximately 30 mm Hg for a period of 4 minutes. The responses of simple and complex cells in the primary visual cortex to visually drifting sinusoidal gratings were measured before and during the elevation of IOP.

results. The response amplitude of all the cortical cells in the primary visual cortex declined during a brief elevation of IOP. The decrease in the response of simple cells was always more significant than that of complex cells. The differential decrease between the two major types of cells was independent of the cell’s receptive field location and cortical depth. There was a mild tendency for cells with higher preferred spatial frequencies to be more sensitive than those with lower frequencies. The preferred orientation and direction of most cortical cells remained roughly unchanged though their orientation and direction biases decreased. An increase in the animal’s blood pressure, which returned the retinal perfusion pressure to a normal level, compensated for the decreased response induced by the elevation of IOP.

conclusions. The differential effects of a brief elevation of IOP on the response of simple and complex cells in the visual cortex are general and may originate from the retina through the lateral geniculate nucleus (LGN), where different effects of elevation of IOP are exerted on X- and Y-type retinal ganglion cells. The results may suggest differential behavior of neurons tin the parvo and magno pathways of the primate.

Maintaining a normal level of intraocular pressure (IOP) is essential in animal and human vision. Elevation of IOP affects visual function by reducing or even completely abolishing the electroretinogram (ERG) and visual evoked potentials (VEPs). 1 2 3 4 The elevation also causes retinal ischemia, interruption of axonal transport, and axonal degeneration, as a result of glaucoma. 5 6 7 8 Abnormalities caused by extreme elevation of IOP may cause blindness. 
Many studies have described the effects of short-term elevation of IOP on the function of the visual system of cats and humans. Most of these studies focused on the effects of elevation of IOP on visual function at population levels, by studying the ERG, VEPs, and optical imaging of brain intrinsic signals. 3 4 9 In some studies, the response properties of single neurons were studied and compared in the retina and the lateral geniculate nucleus (LGN) in the cat, before and during short-term elevation of IOP. 6 10 11 12 Previous work in our laboratory in the cat demonstrated that X-type cells are more sensitive than Y-type cells to brief elevation of IOP, in both the retina and LGN. 10 11 12 Furthermore, the receptive field properties of single neurons in the retina change during high IOP. The surrounding mechanism of a cell’s receptive field in the retina is more susceptible to elevated IOP than is the center mechanism. 11 Evidence has shown that the projections of X and Y cells in LGN to the visual cortex are somewhat dependent on cell class and that the fibers of X cells in the LGN dominate the simple cells and the fibers of Y cells dominate the complex cells 13 14 (for review, see Ref. 15 ). Thus, it is of interest to know whether the responses of different types of cortical neurons vary during elevated IOP. In this study, the response properties of neurons in the primary visual cortex were recorded and compared before and during short-term elevation of IOP, by using single-unit electrophysiological recordings. 
Methods
Surgical Preparation and Physiological Recording
All investigations involving animals adhered to the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research and the Policy of Society for Neuroscience on the Use of Animals in Neuroscience Research. 
The methods used for recording single-unit activity from anesthetized and paralyzed cats have been described elsewhere. 10 11 12 Cats were anesthetized initially with ketamine (25 mg/kg), and surgical anesthesia was continued with intravenous thiopental sodium (0.4 mg/mL). The tracheal and arterial cannulae were inserted, and all pressure points and incisions were infiltrated with a long-acting anesthetic (1% lidocaine HCl). A mixture of gallamine triethiodide (10 mg/kg per hour) and urethane (15 mg/kg per hour) was continuously infused intravenously to maintain anesthesia and paralysis. Electrocardiogram (ECG), electroencephalograph (EEG), and rectal temperature of the animal were monitored throughout the experiments. The end-tidal CO2 was measured and maintained at approximately 4% by adjusting the respirator. The pupils were dilated with atropine (0.5%), and the nictitating membrane was retracted with phenylephrine (2%). The refractive errors of the eyes were tested carefully and corrected appropriately with a contact lens and 3-mm artificial pupils. The eyes were checked routinely to ensure optimum optical conditions before and during elevation of IOP. In general, the difference between the two conditions was less than 0.50 D. In some cases, additional lenses were used for correcting the optics of the eyes if needed. 
The optic nerve head, retinal vessels, and area centralis of the eye were mapped on a sheet of paper covering the screen of the visual stimulator by using the fundus reflective projection method. 16 The primary visual cortex at Horsley-Clarke coordinates P1 to P8 and L0 to L3 was exposed for electrophysiological recording. The action potentials of the cells in the visual cortex were recorded extracellularly with a glass microelectrode. The impedance of microelectrodes ranged from 5 to 15 MΩ. Signals were amplified and passed to an audio monitor and a data collection system (CED micro 1401; Cambridge Electronic Design, Cambridge, UK), with output stored in a computer for analysis (Spike2, ver. 4; Cambridge Electronic Design). 
Elevation of IOP and Blood Pressure
It is known that the function of retinal ganglion cells depends on the ocular perfusion pressure (PP; mean arterial blood pressure minus IOP) rather than the absolute IOP. 6 9 11 To change the ocular PP, we used a method described previously in detail. 9 11 Briefly, a needle was inserted into the anterior chamber of the eye and connected through a cannula to a three-way switch that was connected to a syringe filled with saline and a pressure transducer. Saline was injected into the anterior chamber of the eye to elevate the eye’s IOP. Through a transducer and an analog to digit/digit to analog converter, the resultant IOP was shown on a computer display and adjusted manually to maintain a stable pressure within ±5 mm Hg. The mean arterial blood pressure was monitored continuously throughout the experiment by another blood pressure transducer through a cannula that connected to the femoral artery. Thus, the ocular PP was readily determined. The response of the electroretinogram in the cat decreases with an elevation of IOP and reduction of ocular PP and ceases at a critical PP of approximately 20 mm Hg. 4 Moreover, the response amplitude of intrinsic signal optical imaging maps revealed in visual cortex decreased with the reduction of ocular PP. 9 Therefore, for safety, the minimum PP caused by the elevated IOP we used in the experiments was 30 mm Hg for a period of less than 4 minutes, to minimize detrimental effects of extended elevations of IOP. 
In the three cats studied, by using electrophysiological extracellular recording and optical imaging based on cortical intrinsic signals as described in detail elsewhere, 9 we elevated both the blood pressure and IOP while maintaining a normal ocular PP. To elevate the animal’s blood pressure, metaraminol bitartrate (Aramine, 0.25 mg/mL, 1–2 mL in 3 minutes; Harvest Pharmaceutical Co., Shanghai, China) was injected intravenously so that the mean blood pressure was raised to a level of 180 to 200 mm Hg, and a normal ocular PP was maintained during the elevation of IOP. 
Visual Stimuli
The receptive fields of isolated cortical units were first mapped by using a hand-held target on a tangent screen 57 cm from the cat’s eye. The optic disks were carefully and repeatedly plotted on the screen optically throughout the experiment to ensure that eye movements were prevented completely. Visual stimulus gratings were generated and presented on a computer display (FlexScan F931; EIZO, Ishikawa, Japan) by a stimuli generator (Visual Stimuli Generator 5; Cambridge Research Systems, Ltd., Cambridge, UK). 
Stimulating patterns were drifting sinusoidal gratings presented on a computer display with uniform background of mean luminance 17 cd/m2. The contrast and temporal frequency of the sinusoidal gratings was 50% and 2 Hz, respectively. In each trial, the grating drifted in one direction for 6 seconds. The orientation of each grating used was always orthogonal to the drifting direction. 
After the visual receptive field of a cortical neuron was mapped, the approximate preferred direction and orientation of that cell were determined by a hand-held target. We first measured the spatial frequency-tuning curve for each cell with gratings in a circular area, which was large enough to cover the neuron’s receptive field. Then an orientation-tuning curve was measured in the optimal spatial frequency. The preferred spatial frequency and direction of each cell were used routinely for recording the responses of cells in normal and elevated IOP conditions. 
Data Analysis
Neurons were categorized as simple cells or complex cells according to conventional criteria, such as tests of on/off subregions and dimension of receptive fields, response mode and linearity, and end-stopping. 17 18 19 In addition, relative modulation, the ratio of the amplitude of the first harmonic F1 to the mean response F0 was used for classification. Simple cells appeared to have relative modulations in excess of 1.0, whereas complex cells’ had levels of less than 1.0. 17 18 Because the spontaneous response and ratio of the F1 and F0 components were significantly different between simple and complex cells, the spontaneous response was subtracted beforehand as usual and the mean of firing rate—that is, the total spikes of discharge during one trial divided by 500 ms (2 Hz grating stimuli)—measured from the averaged poststimulus time histograms (PSTHs) were defined as the neuron’s response amplitude (spikes/second) in response to a visual stimulus. Circular statistics, as reported previously, 20 21 22 23 24 were used to quantify the preferred orientation and direction, as well as orientation bias and direction bias, for analyzing the effect of the elevation of IOP on the neural orientation and direction. The responses of each cell to gratings of different orientation (0–180°), drifting in different directions (0–360°), were measured as a series of vectors. The vectors were added and divided by the sum of the absolute values of the vectors. The polar angle of the resultant vector is the cell’s preferred orientation/direction. The length of the resultant vector provides a quantitative measure of orientation bias (OB)/direction bias (DB) of each cell. 
The t-test was used to test for significant differences between the two groups of data. 
Results
Decrease in Response during Elevation of IOP
The responses of single neurons were recorded from the primary visual cortex in different IOP conditions. With an increase of IOP, the responses of almost all cells decreased. A sample of the PSTHs of a simple cell is shown in Figure 1A . For the simple cell, when IOP was progressively elevated from 45 to 80 mm Hg (PP from 65 to 30 mm Hg) the response of the cell decreased gradually and eventually became almost nonexistent (Figs. 1Ac 1Ad) . Only 1 minute after the IOP was returned to the normal level, the response of the cell recovered (Fig. 1Ae) . The mean responses of the simple cell to the different IOP conditions are shown in Figure 1Af . In all the cortical cells we studied, their responses decreased with elevation of IOP; and, once the high IOP was removed, the responses soon recovered. A sample of PSTHs of a complex cell before, during, and after elevation of IOP is also shown in Figure 1B
Difference in Responses of Simple and Complex Cells during Elevation of IOP
The amplitudes of neural response in mean firing rate of 29 simple cells (Fig. 2)and 31 complex cells were compared quantitatively and are shown with normal and elevated IOP (∼80 mm Hg, i.e., PP 30 mm Hg) in Figure 2A . The thin solid line and the dotted line denote the linear regression lines of complex cells (y = 0.68x, r = 0.88) and simple cells (y = 0.47x, r = 0.77), respectively. Obviously, all the data points except two are under the thick solid line of slope 1 (y = x line). Both the slopes of the regression lines were significantly less than 1 (t-test; P < 0.002 for complex cells and P < 0.0002 for simple cells) and the two slopes did not differ significantly (F = 1.2593, t = 1.6147, P < 0.2) indicating that the two types of cortical neurons showed a similar decline in response to an increase in IOP. However, when the mean decreases in responses of the two types of cells were compared (Fig. 2B)at a high level of IOP that caused a PP of 30 mm Hg, the mean relative response of complex cells (59.7% ± 4.2%) was significantly (t-test, P = 0.0002) greater than that of simple cells (35.2% ± 4.5%). Therefore, simple cells were significantly more sensitive than complex cells to elevation of IOP in the primary cortical cortex. 
Responses of Neurons with Different Preferred Spatial Frequencies during Elevation of IOP
Studies in our laboratory demonstrated previously that a selective loss of orientation map elicited by relatively high-spatial-frequency gratings occurs in the visual cortex of the cat during short-term elevations of IOP. 9 Does the effect of elevation of IOP differ in neurons with different preferred spatial frequencies? 
Figure 3shows a histogram of relative responses of cortical cells during elevation of IOP with their optimal spatial frequency. It indicates that elevation in IOP affected simple cells more than complex cells. Moreover, there was a mild tendency for cells with a relatively higher optimal frequency to decrease more in response amplitude than those with a lower optimal frequency, though the difference was not statistically significant in the two groups, because of less and unbalanced sampling. 
Responses of Neurons with Different Eccentricities during Elevation of IOP
The effects of elevation of IOP were compared for neurons with different retinal eccentricity of receptive fields in Figure 4 . Overall, relative response amplitudes of complex cells were larger than those of simple cells at a matched retinal eccentricity within 10° during elevation of IOP; however, these were not statistically significant in two of four groups due to an insufficient sample size. Thus, the difference between simple and complex cortical cells seems independent of the retinal locations from which they receive visual input. 
Effect of Elevating IOP on Cortical Neurons of Different Depths
The effects of the elevation of IOP on cortical function was studied in different layers of the primary visual cortex. Both simple and complex cells were divided into three groups based on their depth in the visual cortex. In Figure 5 , the cortical depths where neurons in groups 1, 2, and 3 were located are defined as those at less than 800 μm (corresponding to layers I, II, and III), between 800 and 1400 μm (layer IV), and more than 1400 μm (layers V and VI), respectively. Given the more simple cells located in layer IV and the more complex cells in other layers, no significant difference in the effect of elevation of IOP was found between the two cell types in each different depth. However, the mean relative responses still suggest a mild difference in the behavior of simple and complex cells in different layers during elevation of IOP. 
Responses of Neurons with Receptive Fields in Different Quadrants
The responses of neurons in different quadrants during an elevation of IOP were recorded and compared in Figure 6 . In these experiments, we counted only the cells recorded from the right cortex with the left eye exposed. For both complex cells and simple cells, the responses of cells whose receptive fields were located in quadrant 1 decreased more significantly (t-test, P < 0.05) than those in quadrants 2, 3, and 4, whereas there was no significant difference in response among all cells whose receptive fields were located in quadrants 2, 3, and 4 (t-test, all P > 0.05) during an elevation of IOP. It revealed that the function of the inferotemporal retina seemed more sensitive to elevation of IOP. Again, no matter what occurred in any of the quadrants, the decrease in the response of simple cells was more significant than that of complex cells, because of elevated IOP. 
Orientation and Direction Selectivity of Neurons
The orientation and direction selectivity of single neurons was tested during elevation of IOP and compared with that obtained in normal IOP. In Figure 7A , during elevation of IOP, the preferred orientation of a complex cell became 107° from 135° in normal IOP, whereas the orientation bias decreased little from 0.24 to 0.18. For the simple cell in Figure 7B , the preferred orientation changed little (from 146° to 138°), and the orientation bias remained almost unchanged (from 0.64 to 0.68; Fig. 7B ). Although the responses of the two types of neurons decreased during elevation of IOP, their preferred orientations did not change. This was true of all 11 cells measured except one (91%), in which the preferred orientation altered more than 22.5° (Fig. 7C) . These results are in agreement with earlier optical imaging data that show that the pattern of orientation columnar maps of a large area of visual cortex remain unchanged during elevation of IOP, although the response amplitude of the orientation maps decreases. 9 In contrast, approximately half of the cells studied (45%, 5/11) changed their preferred directions more than 45° (Fig. 7D) . The preferred direction of cortical neurons was affected by elevation of IOP more than was the preferred orientation. 
The changes in orientation bias and direction bias of cortical cells were compared in the normal and elevated IOP conditions. In Figure 7E , the data in a scatterplot of orientation biases are mainly under the line of slope 1 (y = x), indicating that the orientation bias usually decreased during elevation of IOP. It is likely that there is a greater decrease of the orientation bias in those cells with lower orientation bias than in those with higher bias, because the slope of the dotted regression line is 1.3 larger than 1. Similarly, Figure 7Findicates that the direction bias also decreased during elevation of IOP. However, the decrease in the direction bias seemed more significant in cells with higher direction bias than in those with lower bias, because the slope of the regression line is 0.52 less than 1. 
Effect of Increasing Blood Pressure on the Elevated-IOP–Induced Decrease in Response
In the three cats, we compared the orientation map and neuronal response in the elevated IOP and high blood pressure condition with that of elevated IOP alone (Fig. 8) . In a sample of the experiment in Figure 8A 8B 8C 8D 8E , the high IOP (IOP 110 mm Hg) and reduced retinal PP (10 mm Hg) made the orientation map disappear—that is, the response of the map decreased to zero, a significant change (Fig. 8E ; t-test, P < 10−6). However, as soon as the blood pressure was elevated to 200 mm Hg by an intravenous injection of metaraminol bitartrate (an agent for increasing blood pressure by vasoconstriction), which left the retinal PP near normal level (PP 90 mm Hg), the orientation map retained a relative response of 71% of normal despite the elevated IOP (110 mm Hg). 
In a similar experiment, the high IOP (90 mm Hg) that induced a reduction of retinal PP to 10 mm Hg made the response of the cell decrease to 23% of normal. However, as soon as the blood pressure was elevated to 200 mm Hg by an intravenous injection of metaraminol bitartrate, that left the retinal PP within the normal range (PP 110 mm Hg), the response of the cell soon recovered completely, despite the elevated IOP (90 mm Hg). Taken together, these results indicate that it is the retinal PP, but not the absolute IOP that causes the cortical effect of elevation of IOP that we observed. 
Discussion
The response properties of single neurons were, for the first time, studied in the primary visual cortex in the cat during elevation of IOP. Although both simple and complex cells decreased their response amplitude during an acute increase in IOP, simple cells were affected more significantly than complex cells. This difference was independent of location of the cells’ receptive fields and depth in the cortex, and thus is a general phenomenon in the visual cortex during elevation of IOP. This difference between the two major types of cells during a pathologic condition of elevated IOP is a novel finding in the visual cortex. 
Retinal Origin of the Phenomenon
It is well documented that the effect of brief elevation of IOP on the X cells is more serious than on Y cells, in both the retina and LGN, 10 11 12 and the effect is dependent on the retinal PP but not on the absolute IOP. 6 11 Similarly, a more significant decrease in response amplitude of the orientation maps elicited by high-spatial-frequency gratings than that elicited by low-spatial-frequency gratings was found in the visual cortex of the cat by optical imaging recently, and the decrease are dependent only on the retinal PP in that study as well. 9 In the current study, we found that the single-cell response of the visual cortex decreased markedly during a brief elevation of IOP. The fact that either the orientation map or the cells’ response reappeared with a simultaneously increase in blood pressure strongly indicates a retinal origin of the cortical phenomena observed in the study. 
Simple and complex cells are different in many aspects, such as the size and divisibility of receptive fields, 19 25 26 spontaneous discharge rate, and response mode and linearity, 17 18 27 28 29 as well as sensitivity to motion velocity 25 and to spatial frequency of stimulus gratings. 27 Correspondingly, X and Y types of cells in the retina and LGN of cats have many differences in many receptive field properties similar to those of simple and complex cells. 30 X cells have a small receptive field and respond linearly to fine or higher-spatial-frequency grating stimuli of higher contrast and slow-moving objects. In contrast, Y cells have a larger receptive field and respond nonlinearly to gross and fast-moving objects of low contrast. 31 32 33 Because X type ganglion cells in the retina and relay cells in the dorsal LGN of the cat are more sensitive than the Y cells to a brief elevation of IOP, 10 11 12 it is reasonable to presume that this difference will be reflected in simple and complex cells of the primary visual cortex. 
According to the classic model of Hubel and Wiesel 19 of receptive fields, the receptive field of complex cells was generated from simple-cell convergent inputs in area 17 and not from separated X and Y cell inputs. Accordingly, one would expect that complex cells would be affected by an elevation of IOP as much as or even more than simple cells rather than less. However, the opposite effect was observed in our study. For decades, there has been a longstanding debate about whether simple and complex receptive fields are both constructed from direct geniculate inputs in parallel or serially as in the classic model. The results in the present study seem inconsistent with the speculation based on the classic model and can be readily explained by a bias in Y cell input to complex cells. In fact, there are several lines of evidence based on measurement of conduction velocity of afferents to cat visual cortex showing that simple and complex cells receive predominantly projections from the X- and Y-type cells in the LGN respectively. 13 14 15 Furthermore, most simple cells that behave linearly may receive input from linear X cells, and complex cells that behave nonlinearly from nonlinear Y cells. 17 18 Thus, our results support the argument that even under pathologic conditions, the X cells may predominantly project to simple cells and the Y cells to complex cells. Alternatively, even if complex cells receive only input from simple cells, as suggested by Hubel and Wiesel, 19 the IOP-induced suppression of simple cells may also cause in some complex cells a smaller response decrease than that of simple cells through disinhibition via inhibitory interneurons. Thus, this may be another explanation for our finding of a differential effect of elevated IOP on the two types of cortical cells in the visual cortex. 
The Hubel and Wiesel 19 model of excitatory convergent inputs is usually accepted as an explanation of the generation of significant orientation selectivity of simple cell receptive fields 34 35 36 ; however, intracortical GABAergic inhibition has been reported playing a vital role in forming orientation selectivity. 37 38 39 40 41 A cross-orientation inhibition was also argued to have a role in the forming of orientation selectivity. 42 43 44 Thus, the more complicated intracortical circuits with inhibitory inputs are useful for construction of many simple cell receptive fields. However, until recently, there had been no anatomic evidence supporting the Hubel and Wiesel 19 model for the past 40 years. Zhan and Shou 45 provided the first anatomic evidence for it and indicated that this mechanism exists but may not be a common one; in fact, it may be quite rare. Besides, most neurons in the dorsal LGN are already orientation sensitive. 46 47 48 49 50 Overall, it is likely that multiple mechanisms rather than the single mechanism of the Hubel and Wiesel model contribute to the receptive fields of various cortical cells. 
Spatial Frequency Dependence
Our results suggest that cortical neurons with lower preferred spatial frequency tend to be more tolerant than those with higher preferred spatial frequency. This finding is in agreement with the optical imaging observation that the selective loss of the orientation map elicited by a high-spatial-frequency grating occurs in a large area of the visual cortex 9 and that the responses of X cells decrease more significantly than those of Y cells in the retina and LGN 10 11 12 during a brief elevation of IOP. Correspondingly, X cells are responsible predominantly for fine vision with high spatial frequency information, whereas Y cells are responsible more for gross vision and motion discrimination. Moreover, the receptive fields of most cells sensitive to high spatial frequency are concentrated in the central visual field, and the density of X cells is much higher than Y cells in the central retina. This also explains the quick decline of visual acuity of patients with acute angle-closure glaucoma. 51  
Possible Contribution of Area 18
The visual cortex exposed in the experiments was at Horsley-Clarke coordinates P1 to P8 and L1 to L3, located in area 17 according to the topographic atlas of the cat. However, because the topographic locations of areas 17 and 18 are largely varied between the cats tested, we do not exclude the possibility that area 18 is also involved in the cell-type differential effect of an elevation of IOP. Because in the cat area 17 receives X and Y inputs from the LGN, whereas area 18 receives predominantly Y input 13 14 15 and the X cells are more sensitive than Y cells to elevation of IOP in the retina and the LGN, 10 11 12 the decrease of most neural responses in area 18 during elevation of IOP should be smaller than those in area 17. Furthermore, given the quantitative measure that cells in the feline area 17 respond preferentially to spatial frequencies (>0.3 cyc/deg) greater than those in area 18 (<0.3 cyc/deg) 27 and the spatial-frequency-selective loss of orientation maps during an elevation of IOP, 9 and considering the tendency we found in this study that cells with low preferred spatial frequencies tend to be better tolerated than those with high preferred spatial frequencies to elevation of IOP, the results should also reflect the different effects that an elevation of IOP may have on cortical neurons in areas 17 and 18, if our observation includes area 18. 
Comparison of Effects between Acute and Chronic Elevation of IOP
A large amount of evidence has shown that chronic elevation of IOP during glaucoma causes a progressive degeneration of optic nerve fibers and loss of retinal ganglion cells. These changes are cell-type dependent (i.e., large cells are damaged selectively greater than small cells). 51 52 53 54 55 56 Recent work in our laboratory has demonstrated that in cats with chronic glaucoma, large α (Y) cells remaining in the retina shrink more than small β (X) cells in dendritic structures including the dendritic field diameter, total length, and bifurcations of dendrites, in addition to having a loss of retinal ganglion cells. 57 The phenomena observed in chronic glaucoma are opposite those we have found in retina, the LGN, and in the visual cortex during acute elevations of IOP, 10 11 12 suggesting possible different mechanisms underlying these findings. This difference may be caused by different lengths and magnitudes of IOP used in experiments of acute and chronic elevation of IOP. In the acute experiments, IOP was elevated to a very high level in a short period (a few minutes), whereas in chronic experiments the IOP was relatively low and maintained for a long period (a few weeks or months). Y cells, due to their large size may be better in demonstrating resistance to the brief depravation of oxygen, glucose, and adenosine triphosphate (ATP) supplied by the retinal blood, 58 but may be worse in surviving and maintaining normal function over a long period of elevation of IOP, presumably due to their larger consumption (or size), higher contrast sensitivity, greater susceptibility to neurotoxicosis, and higher sensitivity to mechanical pressure. 59 60 61  
The IOP used in this study was elevated to a critical level (80–100 mm Hg) that caused a PP of 30 mm Hg. The eye condition was similar to that of acute angle-closure glaucoma at the breaking-out stage, which results in a sharp decrease in visual acuity and rapid blindness. Thus, this study provides the first observation of differential behavior of two major types of cortical cells and a way to study cortical mechanisms of glaucoma during an acute elevation of IOP. 
 
Figure 1.
 
The responses of a simple (A) and a complex (B) cell to visual grating stimuli before, during, and after brief elevation of IOP. (Aa) PSTH of responses of a simple cell when the IOP was normal (10 mm Hg). (AbAd) PSTHs when IOP was at 45, 60, and 80 mm Hg, respectively. (Ae) PSTH when IOP returned to normal. Each PSTH in (Ab), (Ac), and (Ad) was measured under different elevations of IOP and then after return to normal (Ae), which occurred within 10 to 30 minutes. (Af) Mean responses of the cell under conditions in (AaAe). It is clear that, with the elevation of IOP, the response of the cell decreased gradually and recovered when high IOP ended. (Ba) PSTH of responses of a complex cell when the IOP was normal (10 mm Hg), (Bb) when it was at 80 mm Hg, and (Bc) it returned to normal. (Bd) Mean responses of the cell under conditions in (BaBd). Note that the complex cell continued to have relatively more discharges than the simple cell during identical elevations of IOP to 80 mm Hg. The spatial frequency of the gratings used was 0.8 and 0.2 cyc/deg for the simple and the complex cells, respectively, and the temporal frequency was 2 Hz.
Figure 1.
 
The responses of a simple (A) and a complex (B) cell to visual grating stimuli before, during, and after brief elevation of IOP. (Aa) PSTH of responses of a simple cell when the IOP was normal (10 mm Hg). (AbAd) PSTHs when IOP was at 45, 60, and 80 mm Hg, respectively. (Ae) PSTH when IOP returned to normal. Each PSTH in (Ab), (Ac), and (Ad) was measured under different elevations of IOP and then after return to normal (Ae), which occurred within 10 to 30 minutes. (Af) Mean responses of the cell under conditions in (AaAe). It is clear that, with the elevation of IOP, the response of the cell decreased gradually and recovered when high IOP ended. (Ba) PSTH of responses of a complex cell when the IOP was normal (10 mm Hg), (Bb) when it was at 80 mm Hg, and (Bc) it returned to normal. (Bd) Mean responses of the cell under conditions in (BaBd). Note that the complex cell continued to have relatively more discharges than the simple cell during identical elevations of IOP to 80 mm Hg. The spatial frequency of the gratings used was 0.8 and 0.2 cyc/deg for the simple and the complex cells, respectively, and the temporal frequency was 2 Hz.
Figure 2.
 
(A) Comparison of neuronal response amplitudes (mean firing rate) in normal IOP versus those in high IOP (PP 30 mm Hg). Most data points are located under the thick solid line of slope 1, indicating a significant decrease in visual responses due to elevated IOP. (B) Statistical comparison in relative response of different types of cells. The relative response amplitude is defined as the neuronal response during high IOP divided by the response during normal IOP. The relative responses of complex and simple cells during elevation of IOP were significantly different. **P < 0.0005.
Figure 2.
 
(A) Comparison of neuronal response amplitudes (mean firing rate) in normal IOP versus those in high IOP (PP 30 mm Hg). Most data points are located under the thick solid line of slope 1, indicating a significant decrease in visual responses due to elevated IOP. (B) Statistical comparison in relative response of different types of cells. The relative response amplitude is defined as the neuronal response during high IOP divided by the response during normal IOP. The relative responses of complex and simple cells during elevation of IOP were significantly different. **P < 0.0005.
Figure 3.
 
The effect of elevation of IOP on neurons with different preferred spatial frequencies. The relative responses of complex cells were higher than those of simple cells during elevated IOP. For both types of cells in most cases, the relative responses during high IOP were lesser in cells with high preferred spatial frequency than in those with low preferred frequencies. *Significant difference between the two groups; P < 0.05.
Figure 3.
 
The effect of elevation of IOP on neurons with different preferred spatial frequencies. The relative responses of complex cells were higher than those of simple cells during elevated IOP. For both types of cells in most cases, the relative responses during high IOP were lesser in cells with high preferred spatial frequency than in those with low preferred frequencies. *Significant difference between the two groups; P < 0.05.
Figure 4.
 
Relative responses of cortical cells with receptive fields at different retinal eccentricity. The effects of elevated IOP on the two types of cells were significantly different due to insufficient sampling for each group. *Significant difference between the two groups; P < 0.05.
Figure 4.
 
Relative responses of cortical cells with receptive fields at different retinal eccentricity. The effects of elevated IOP on the two types of cells were significantly different due to insufficient sampling for each group. *Significant difference between the two groups; P < 0.05.
Figure 5.
 
Relative responses of cortical neurons located at different depths in the visual cortex. All the cells are divided into three groups according to location in the cortical cortex relative to the pial surface: <800 μm, 800–1400 μm, and >1400 μm. The differential effect of elevation of IOP in the different cell types existed despite the cell’s location.
Figure 5.
 
Relative responses of cortical neurons located at different depths in the visual cortex. All the cells are divided into three groups according to location in the cortical cortex relative to the pial surface: <800 μm, 800–1400 μm, and >1400 μm. The differential effect of elevation of IOP in the different cell types existed despite the cell’s location.
Figure 6.
 
Relative responses of neurons with receptive fields (RF) located in different quadrants of the visual field during elevation of IOP. No complex cell recorded had a receptive field within quadrant 2 of the visual field. The effects of elevated IOP were cell-type dependent, regardless of the cell’s receptive field location.
Figure 6.
 
Relative responses of neurons with receptive fields (RF) located in different quadrants of the visual field during elevation of IOP. No complex cell recorded had a receptive field within quadrant 2 of the visual field. The effects of elevated IOP were cell-type dependent, regardless of the cell’s receptive field location.
Figure 7.
 
Effects of elevation of IOP on orientation and direction sensitivity of cells in the visual cortex. (A, B) Direction/orientation-tuning curves of one complex (A) cell and one simple (B) cell, before and during elevation of IOP. The orientation of the drifting gratings was orthogonal to the direction of motion. Distribution of change in the preferred orientation (C) and direction (D) of cortical cells during normal and elevated IOP. Although the preferred direction changed significantly during elevation of IOP, the preferred orientation changed little. (E) Comparison of orientation biases of cortical cells during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = −0.32 + 1.3x; r = 0.89; P < 0.0005). (F) Comparison of direction biases during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = 0.089 + 0.52x; r = 0.73; P = 0.01).
Figure 7.
 
Effects of elevation of IOP on orientation and direction sensitivity of cells in the visual cortex. (A, B) Direction/orientation-tuning curves of one complex (A) cell and one simple (B) cell, before and during elevation of IOP. The orientation of the drifting gratings was orthogonal to the direction of motion. Distribution of change in the preferred orientation (C) and direction (D) of cortical cells during normal and elevated IOP. Although the preferred direction changed significantly during elevation of IOP, the preferred orientation changed little. (E) Comparison of orientation biases of cortical cells during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = −0.32 + 1.3x; r = 0.89; P < 0.0005). (F) Comparison of direction biases during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = 0.089 + 0.52x; r = 0.73; P = 0.01).
Figure 8.
 
The recovery of orientation maps (AE) in one cat and a neuron’s responses (FI) in another cat, caused by increasing the animal’s blood pressure during elevation of IOP. (A, C) Orientation maps of a cat’s primary visual cortex revealed by intrinsic signal optical imaging when a drifting grating was used as a stimulus during normal IOP. (B) Orientation map with an IOP of 110 mm Hg and (D) when the blood pressure was pharmacologically increased to 200 mm Hg with an IOP of 110 mm Hg (PP 90 mm Hg). (E) Response amplitudes (mean ± SD) of orientation maps (AD) in various conditions. (FH) PSTHs recorded from a neuron in the primary visual cortex responding to drifting grating stimuli in the normal IOP (F), during IOP of 90 mm Hg (G), and during IOP of 90 mm Hg with arterial blood pressure increased to 200 mm Hg (H), which resulted in a normal level of retinal PP (110 mm Hg). (I) Mean responses of this neuron in conditions in (F), (G), and (H).
Figure 8.
 
The recovery of orientation maps (AE) in one cat and a neuron’s responses (FI) in another cat, caused by increasing the animal’s blood pressure during elevation of IOP. (A, C) Orientation maps of a cat’s primary visual cortex revealed by intrinsic signal optical imaging when a drifting grating was used as a stimulus during normal IOP. (B) Orientation map with an IOP of 110 mm Hg and (D) when the blood pressure was pharmacologically increased to 200 mm Hg with an IOP of 110 mm Hg (PP 90 mm Hg). (E) Response amplitudes (mean ± SD) of orientation maps (AD) in various conditions. (FH) PSTHs recorded from a neuron in the primary visual cortex responding to drifting grating stimuli in the normal IOP (F), during IOP of 90 mm Hg (G), and during IOP of 90 mm Hg with arterial blood pressure increased to 200 mm Hg (H), which resulted in a normal level of retinal PP (110 mm Hg). (I) Mean responses of this neuron in conditions in (F), (G), and (H).
The authors thank Robert S. Litman for careful editing of the manuscript. 
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Figure 1.
 
The responses of a simple (A) and a complex (B) cell to visual grating stimuli before, during, and after brief elevation of IOP. (Aa) PSTH of responses of a simple cell when the IOP was normal (10 mm Hg). (AbAd) PSTHs when IOP was at 45, 60, and 80 mm Hg, respectively. (Ae) PSTH when IOP returned to normal. Each PSTH in (Ab), (Ac), and (Ad) was measured under different elevations of IOP and then after return to normal (Ae), which occurred within 10 to 30 minutes. (Af) Mean responses of the cell under conditions in (AaAe). It is clear that, with the elevation of IOP, the response of the cell decreased gradually and recovered when high IOP ended. (Ba) PSTH of responses of a complex cell when the IOP was normal (10 mm Hg), (Bb) when it was at 80 mm Hg, and (Bc) it returned to normal. (Bd) Mean responses of the cell under conditions in (BaBd). Note that the complex cell continued to have relatively more discharges than the simple cell during identical elevations of IOP to 80 mm Hg. The spatial frequency of the gratings used was 0.8 and 0.2 cyc/deg for the simple and the complex cells, respectively, and the temporal frequency was 2 Hz.
Figure 1.
 
The responses of a simple (A) and a complex (B) cell to visual grating stimuli before, during, and after brief elevation of IOP. (Aa) PSTH of responses of a simple cell when the IOP was normal (10 mm Hg). (AbAd) PSTHs when IOP was at 45, 60, and 80 mm Hg, respectively. (Ae) PSTH when IOP returned to normal. Each PSTH in (Ab), (Ac), and (Ad) was measured under different elevations of IOP and then after return to normal (Ae), which occurred within 10 to 30 minutes. (Af) Mean responses of the cell under conditions in (AaAe). It is clear that, with the elevation of IOP, the response of the cell decreased gradually and recovered when high IOP ended. (Ba) PSTH of responses of a complex cell when the IOP was normal (10 mm Hg), (Bb) when it was at 80 mm Hg, and (Bc) it returned to normal. (Bd) Mean responses of the cell under conditions in (BaBd). Note that the complex cell continued to have relatively more discharges than the simple cell during identical elevations of IOP to 80 mm Hg. The spatial frequency of the gratings used was 0.8 and 0.2 cyc/deg for the simple and the complex cells, respectively, and the temporal frequency was 2 Hz.
Figure 2.
 
(A) Comparison of neuronal response amplitudes (mean firing rate) in normal IOP versus those in high IOP (PP 30 mm Hg). Most data points are located under the thick solid line of slope 1, indicating a significant decrease in visual responses due to elevated IOP. (B) Statistical comparison in relative response of different types of cells. The relative response amplitude is defined as the neuronal response during high IOP divided by the response during normal IOP. The relative responses of complex and simple cells during elevation of IOP were significantly different. **P < 0.0005.
Figure 2.
 
(A) Comparison of neuronal response amplitudes (mean firing rate) in normal IOP versus those in high IOP (PP 30 mm Hg). Most data points are located under the thick solid line of slope 1, indicating a significant decrease in visual responses due to elevated IOP. (B) Statistical comparison in relative response of different types of cells. The relative response amplitude is defined as the neuronal response during high IOP divided by the response during normal IOP. The relative responses of complex and simple cells during elevation of IOP were significantly different. **P < 0.0005.
Figure 3.
 
The effect of elevation of IOP on neurons with different preferred spatial frequencies. The relative responses of complex cells were higher than those of simple cells during elevated IOP. For both types of cells in most cases, the relative responses during high IOP were lesser in cells with high preferred spatial frequency than in those with low preferred frequencies. *Significant difference between the two groups; P < 0.05.
Figure 3.
 
The effect of elevation of IOP on neurons with different preferred spatial frequencies. The relative responses of complex cells were higher than those of simple cells during elevated IOP. For both types of cells in most cases, the relative responses during high IOP were lesser in cells with high preferred spatial frequency than in those with low preferred frequencies. *Significant difference between the two groups; P < 0.05.
Figure 4.
 
Relative responses of cortical cells with receptive fields at different retinal eccentricity. The effects of elevated IOP on the two types of cells were significantly different due to insufficient sampling for each group. *Significant difference between the two groups; P < 0.05.
Figure 4.
 
Relative responses of cortical cells with receptive fields at different retinal eccentricity. The effects of elevated IOP on the two types of cells were significantly different due to insufficient sampling for each group. *Significant difference between the two groups; P < 0.05.
Figure 5.
 
Relative responses of cortical neurons located at different depths in the visual cortex. All the cells are divided into three groups according to location in the cortical cortex relative to the pial surface: <800 μm, 800–1400 μm, and >1400 μm. The differential effect of elevation of IOP in the different cell types existed despite the cell’s location.
Figure 5.
 
Relative responses of cortical neurons located at different depths in the visual cortex. All the cells are divided into three groups according to location in the cortical cortex relative to the pial surface: <800 μm, 800–1400 μm, and >1400 μm. The differential effect of elevation of IOP in the different cell types existed despite the cell’s location.
Figure 6.
 
Relative responses of neurons with receptive fields (RF) located in different quadrants of the visual field during elevation of IOP. No complex cell recorded had a receptive field within quadrant 2 of the visual field. The effects of elevated IOP were cell-type dependent, regardless of the cell’s receptive field location.
Figure 6.
 
Relative responses of neurons with receptive fields (RF) located in different quadrants of the visual field during elevation of IOP. No complex cell recorded had a receptive field within quadrant 2 of the visual field. The effects of elevated IOP were cell-type dependent, regardless of the cell’s receptive field location.
Figure 7.
 
Effects of elevation of IOP on orientation and direction sensitivity of cells in the visual cortex. (A, B) Direction/orientation-tuning curves of one complex (A) cell and one simple (B) cell, before and during elevation of IOP. The orientation of the drifting gratings was orthogonal to the direction of motion. Distribution of change in the preferred orientation (C) and direction (D) of cortical cells during normal and elevated IOP. Although the preferred direction changed significantly during elevation of IOP, the preferred orientation changed little. (E) Comparison of orientation biases of cortical cells during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = −0.32 + 1.3x; r = 0.89; P < 0.0005). (F) Comparison of direction biases during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = 0.089 + 0.52x; r = 0.73; P = 0.01).
Figure 7.
 
Effects of elevation of IOP on orientation and direction sensitivity of cells in the visual cortex. (A, B) Direction/orientation-tuning curves of one complex (A) cell and one simple (B) cell, before and during elevation of IOP. The orientation of the drifting gratings was orthogonal to the direction of motion. Distribution of change in the preferred orientation (C) and direction (D) of cortical cells during normal and elevated IOP. Although the preferred direction changed significantly during elevation of IOP, the preferred orientation changed little. (E) Comparison of orientation biases of cortical cells during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = −0.32 + 1.3x; r = 0.89; P < 0.0005). (F) Comparison of direction biases during normal and elevated IOP. Solid line: slope 1 (y = x); dotted line: linear regression line of cells tested (y = 0.089 + 0.52x; r = 0.73; P = 0.01).
Figure 8.
 
The recovery of orientation maps (AE) in one cat and a neuron’s responses (FI) in another cat, caused by increasing the animal’s blood pressure during elevation of IOP. (A, C) Orientation maps of a cat’s primary visual cortex revealed by intrinsic signal optical imaging when a drifting grating was used as a stimulus during normal IOP. (B) Orientation map with an IOP of 110 mm Hg and (D) when the blood pressure was pharmacologically increased to 200 mm Hg with an IOP of 110 mm Hg (PP 90 mm Hg). (E) Response amplitudes (mean ± SD) of orientation maps (AD) in various conditions. (FH) PSTHs recorded from a neuron in the primary visual cortex responding to drifting grating stimuli in the normal IOP (F), during IOP of 90 mm Hg (G), and during IOP of 90 mm Hg with arterial blood pressure increased to 200 mm Hg (H), which resulted in a normal level of retinal PP (110 mm Hg). (I) Mean responses of this neuron in conditions in (F), (G), and (H).
Figure 8.
 
The recovery of orientation maps (AE) in one cat and a neuron’s responses (FI) in another cat, caused by increasing the animal’s blood pressure during elevation of IOP. (A, C) Orientation maps of a cat’s primary visual cortex revealed by intrinsic signal optical imaging when a drifting grating was used as a stimulus during normal IOP. (B) Orientation map with an IOP of 110 mm Hg and (D) when the blood pressure was pharmacologically increased to 200 mm Hg with an IOP of 110 mm Hg (PP 90 mm Hg). (E) Response amplitudes (mean ± SD) of orientation maps (AD) in various conditions. (FH) PSTHs recorded from a neuron in the primary visual cortex responding to drifting grating stimuli in the normal IOP (F), during IOP of 90 mm Hg (G), and during IOP of 90 mm Hg with arterial blood pressure increased to 200 mm Hg (H), which resulted in a normal level of retinal PP (110 mm Hg). (I) Mean responses of this neuron in conditions in (F), (G), and (H).
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