Abstract
purpose. To investigate the effect of ageing on contour integration in subjects whose ages ranged from 20 to 99 years.
methods. Detection thresholds were measured for a closed chain of Gabor patches oriented tangentially to a circle (target) embedded in a background of randomly positioned and oriented Gabors (noise). Detection thresholds were measured for different distances of elements composing the target.
results. Sensitivity decreases gradually with age at all interelement distances. Sensitivity decreases with increasing interelement distance, in both young and elderly subjects. The decrease of integration capability with age is not related to a decrease in contrast sensitivity.
conclusions. Overall, the data provide evidence of a deterioration of cortical functionality with age, in agreement with other studies on texture and motion processing.
Visual abilities decline during normal (nonpathologic) ageing, but our understanding of the nature and causes of visual changes in the elderly is still limited. Damages to optical properties of the eyes (e.g., presbyopia, senile miosis) are the most common cause of visual deficits in the old population, producing deterioration of low-level visual functions, such as visual acuity and contrast sensitivity.
1 2 3 However, visual acuity reduction is not exclusively due to changes in the eye’s optical properties.
4 5 6 7 Ageing produces loss of photoreceptor, bipolar, or ganglion cells and changes in their connections that could account for visual acuity losses.
8 9 The decrease in contrast sensitivity observed with ageing (for frequencies higher than 2 cyc/deg),
10 is also due to a natural deterioration of optical properties,
11 12 as well as to retinal or central visual damage Zuckermann JL et al.
IOVS 1973;12:ARVO Abstract 213)
4 13 14 15 16 Porciatti et al.
17 found small differences in PERG, whereas VEP amplitudes and phases of old subjects were lower than those of young subjects, suggesting that visual impairment in the elderly occurs primarily in V1. More in general, ageing affects PERG and VEPs at low temporal frequencies, producing lower amplitudes and increased latency, particularly at high spatial frequencies.
17 18 19 20 21 Despite the well-documented anatomic and physiological age-related changes in the primary visual pathway, the extent to which they contribute to specific nonpathologic deficits in low-level visual function remains unresolved.
22
If our understanding of age-related changes in low-level processes is limited, it is also true that not much is known about the effects of ageing on the way neurons elaborate and integrate complex information from the external environment and about the relationship between behavior and diminished neural functions. There are several studies indicating a decreased activity in the ageing brain related to high-level cognitive tasks. Measurements of cerebral blood flow (rCBF) by standard positron emission tomography (PET) reveal differences in activation between young and old subjects in object-recognition tasks,
23 24 face recognition,
25 and stimulus encoding.
26
In some recent studies, investigators have begun to examine also the consequences of ageing on visual perception, finding some abilities to be particularly affected by ageing whereas others are relatively spared. Snowden and Kavanagh
27 have explored several aspects of motion perception and found a variety of deficits not accompanied by a significant loss in contrast sensitivity. These deficits were ascribed to a deterioration of the brain areas responsible for global motion perception, such as the medial temporal area.
28 29 30 O’Brien et al.
31 also found a diminished sensitivity to optic flow motion in healthy elderly subjects. Changes due to ageing do not necessarily bring about a deterioration of visual function. Some investigators have found that motion perception of large, high-contrast stimuli is even better in old subjects than in young adults.
32 This effect was attributed to age-related reductions in GABA-mediated inhibition
33 that, while having a detrimental effect on a broad range of cognitive, perceptual, and behavioral functions, could weaken center-surround antagonism and increase performance in motion perception.
34 Some studies report particularly low performance of the elderly in midlevel tasks, such as bilateral symmetry detection,
35 and in tasks requiring high-level or second-order processing, such as second-order motion and texture,
36 in comparison with tasks requiring first-order processing. These results led the authors to formulate the hypothesis that deficits in perceptual processing due to ageing become evident when the computational load of the task reaches a certain level of complexity, requiring larger or more complex networks that are not available in the ageing brain.
37
Contour integration is a complex ability, widely investigated in multiple-choice detection tasks, in which a chain of Gabor patches (GPs)—sinusoidal luminance signals within a Gaussian envelope—must be segregated from a noisy background.
38 39 40 In these stimuli, there is no global cue—orientation, color, or texture—for the segregation of the chain. The global patterns seem to emerge from interactions between local mechanisms, influenced by variables such as relative orientation of nearby cues, relative distance, and colinearity.
38 41 42 43 In particular, the critical distance between GPs that allows integration to occur for a given stimulus is a crucial parameter and may be related to connections between simple cortical units.
41 44 In fact, several lines of anatomic,
45 46 47 physiological,
48 49 and imaging
50 evidence suggest that horizontal connections can link cells with nonoverlapping receptive fields, with similar orientation preferences, as early as in V1.
This contour segregation ability, which is part of a more general task of figure-ground segmentation,
39 is a second-order task, involving integration of locally oriented elements in a global percept. This task would require larger networks that, according to some investigators,
37 could generate age-related deficits. A multiple-stage analysis could also explain why this ability undergoes protracted development during childhood.
51 52 It is therefore interesting to study contour integration during ageing to verify whether the complexity of the task affects visual performance in the elderly.
The knowledge of natural evolution of contour integration during ageing is also useful to discriminate the normal trend in the ageing brain from a deterioration of this ability observed in some degenerative diseases.
53
In this study, we measured how visual integration ability changes with age, by measuring detection thresholds of a closed chain of GPs, oriented tangentially to a circle (target), embedded in a dense field of Gabors oriented randomly (noise), at different ages. We also tested whether in older people there is the same dependency on interelement distance in the target observed in younger subjects.
38
The presentation of the stimuli was always preceded by a sound to catch the subjects’ attention. The target could be positioned randomly in one of four quadrants of the computer screen
(Fig. 1) , and the subject’s task was to locate the circle with a four-alternative, forced-choice procedure. Responses were reported verbally by the subjects and recorded manually by the experimenter. The subjects had no time limit for response, and no verbal or sound feedback was given.
For each separation between GPs comprising the target, the integration ability was quantified by measuring detection thresholds for the circular target, varying the number of noise GPs. Target-detection thresholds were defined by the number of noise GPs yielding 75% correct detection.
To minimize tiredness and boredom, data on elderly subjects were obtained in four sessions on different days, each of them measuring all conditions. Data on younger subjects were obtained in four sessions on the same day. We checked that the different data-taking procedures do not affect the results, by repeating some measurements on young subjects with the same method used on elderly subjects. The measurements obtained in these two manners were compatible at the 95% confidence level. Data for each condition were collected in five blocks of 30 trials. In each block, the number of noise Gabors was varied along different trials according to a staircase QUEST procedure.
54
For every tested condition and for each subject, a cumulative maximum-likelihood fit was performed off-line with all data obtained in all sessions, by using a Weibull psychometric function.
55 Thresholds were defined as the point of the fitting curve where probability of correct response equals 0.75. We plotted sensitivities rather than thresholds, to represent and compare performances. Sensitivity is defined as (S+N)/S where S is the number of target GPs, and N is the number of noise GPs at threshold.
Contrast sensitivities were measured with a portable test chart system (VCTS 6000; Vistech Consultants, Dayton, OH). For all subjects, young and old, environmental luminance level was kept constant around 115 cd/m2, and test charts were positioned 46 cm away from subjects by using an apposite chart-holder. Contrast sensitivity curves were obtained for spatial frequencies of 1.5, 3, 6, 12, and 18 cyc/deg. Each measurement is the average of three different trials.
Dependence of sensitivity on age was estimated fitting data with a straight line. Statistical significance of angular coefficients obtained from fit was tested with normal distribution tests
(Table 1) , used also to test differences between them. Dependence of average performance on integration distance and group was tested with two-way ANOVA (with Bonferroni correction). Post hoc Student’s
t-tests were used to compare performances of old and young subjects
(Table 1) . Dependence of contrast sensitivity on age was also estimated fitting data at a particular frequency with a straight line.
The young sample was composed of 11 observers (mean age, 25 ± 1 years; range, 24–27), and the elderly sample comprised 21 observers (mean age, 65 ± 8 years, range, 51–83). We also tested one observer who was 99 years old, well outside the range (subject GB). Younger subjects were middle-class Italian university students, and the older subjects were selected among their relatives (i.e., grandparents, uncles) in good general health, and living in the same area. All subjects had normal or corrected-to-normal vision with their glasses or contact lenses. Old subjects did not have eye defects (such as cataract and glaucoma) or neurologic deficits such as Alzheimer disease or other forms of dementia associated with age. Both experimental groups had similar socioeconomic status and educational background. The measurement of contrast sensitivity was performed in a later session (2 weeks later) in which 6 young and 15 old subjects from the initial group were available.
This research adhered to the tenets of the Declaration of Helsinki, and informed consent was obtained from all subjects after explanation of the nature and possible consequences of the study.
In the present study contour integration ability deteriorated during ageing. In fact, sensitivity for detection of a target composed of local elements, embedded in a noise field, decreased linearly with age, independent of the distance between local elements. One could argue whether the observed handicap in old people is purely perceptual or is caused by high-level cognitive ageing factors, such as less efficient search strategies, or by nonvisual factors, such as reduced motivation in completing a difficult task. Our data cannot rule out these possibilities, but the adopted procedure—limited presentation time, guessing factor of 25%—limits the influence of visual search in completing the task. The repetition of the same measurement—one for each distance—on five different days was a control for motivation.
In both age groups, contour integration deteriorated, as distance between local elements comprising the target increased, in agreement with previous studies in which improved performance was found with colinearity and proximity.
38 41 42 43 However, the performance at short distances seemed to be more affected by age
(Table 1) .
Recently, some investigators devised a hypothesis to explain why some perceptual abilities are more affected by ageing than others.
35 36 37 56 They suggest the magnitude of the observed age-related changes depends on stimulus complexity (given by the computational load or by the complexity of the underlying neural network). Our data are consistent only in part with this hypothesis: contour integration ability, which is a second-order complex task, is diminished with age, but age-related changes are more pronounced at shorter distances, when the task appears to be easier. These counter-intuitive results could be explained with different integration mechanisms, for large and small contour spacing, that evolve separately during life
51 and are affected differently by ageing.
Elderly subjects who participated in our experiments were healthy, active, and independent, with contrast sensitivity within the norm of their age—therefore, without significant low-level deficits—nevertheless, we found a natural decline in contrast sensitivity with age. In the current study we demonstrate that there was no correlation between contrast sensitivity and integration sensitivity, when corrected for age dependency. Therefore, the observed impairment with ageing in contour integration cannot be due to ageing of the neural circuits that underlie contrast sensitivity, the precise localization of which remain unknown, occurring at any level between the retina and the visual cortex.
4 15
The exact localization of the circuits responsible for spatial integration of colinear elements over a certain distance is also still largely unknown. Many studies have demonstrated that long-range connections in the striate cortex, localized in the plexus of intrinsic horizontal connections of V1,
46 57 58 59 60 connect cells with similar orientation preference.
61 These connections could be altered in elderly individuals and, in principle, could be responsible for the observed deficit. These connections are not solely responsible for the contour-detection task, which may be modulated by feedback top-down connections originating in the extrastriate cortex. In particular, for global processing, functional neuroimaging studies have located the source of such a modulatory activity in the right temporoparietal junction.
62 Other neurophysiological findings provide evidence of the existence of facilitatory top-down effects that could amplify and focus the activity of neurons in lower-order areas and thus facilitate figure-ground segmentation and improve the visibility of features and contribute to the “pop-out” phenomenon.
63 Studies of the development of the visual system
64 suggest also a role of feedback connections from V2 to V1 in contour integration.
51 Although the lateral and feedback connections of V1 are essential in completing a contour-detection task, cortical areas concerned with form vision, such as V4,
65 probably also participate in this process. Given the complexity of circuits and areas involved in the contour-detection task, the anatomic substrates of modifications induced by ageing have yet to be identified.
Regarding the nature of modifications of these circuits, several studies have found in the ageing brain changes in neuronal discharges, neurotransmitter release, and response to neurotransmitters.
33 66 67 68 69 70 71 In the visual system, ageing produces the loss of retinal cells
8 9 ; selective damage to the parvocellular pathway, perhaps related to changes in spatial contrast sensitivity
72 73 ; abnormal dendritic growth; dendritic regression; and reduction of the spinal density of striate cortex cells.
74 75 76 Recent work provides evidence that both the orientation and direction selectivities of extrastriate V2 cells in old monkeys degrade significantly while spontaneous activity increases.
77 These modifications could underlie the decline in higher-order visual functions, such as contour integration, occurring during ageing. However, there is no direct evidence that similar modifications occur in the striate and extrastriate cortex of humans, and our understanding of the effects of ageing on the neuronal circuitry attributed to contour integration remains rudimentary.
Submitted for publication June 29, 2006; revised December 12, 2006; accepted April 19, 2007.
Disclosure:
M.M. Del Viva, None;
R. Agostini, None
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked “
advertisement” in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Corresponding author: Maria Michela Del Viva, Istituto di Neuroscienze, CNR Area di Ricerca di Pisa via Moruzzi 1 56100 Pisa, Italy;
[email protected].
Table 1. Decline in Sensitivity with Age at Different GP Separations
Table 1. Decline in Sensitivity with Age at Different GP Separations
Distance | α | σ | P (α = 0) |
4.9° | −0.079 | 0.017 | <0.00001 |
3.8° | −0.082 | 0.018 | <0.00001 |
2.9° | −0.126 | 0.020 | <0.00001 |
2.1° | −0.216 | 0.035 | <0.00001 |
Table 2. Mean Sensitivities of the Two Samples of Subjects for Each Interelement Distance
Table 2. Mean Sensitivities of the Two Samples of Subjects for Each Interelement Distance
Distance | Young Subjects | | Old Subjects | | P * |
| Mean | SD | Mean | SD | |
4.9° | 9.2 | 2.6 | 6.4 | 1.7 | <0.00059 |
3.8° | 10.3 | 2.8 | 7.2 | 1.8 | <0.00001 |
2.9° | 13.4 | 2.9 | 8.5 | 2.1 | <0.00088 |
2.1° | 21.3 | 6.0 | 11.7 | 1.7 | <0.00089 |
The authors thank Concetta Morrone and David Burr for helpful discussions.
ElliotDB, WhitakerD, MacFeighD. Neural contribution to spatiotemporal contrast sensitivity decline in healthy ageing eyes. Vision Res. 1990;30:541–547.
[CrossRef] [PubMed]PittsD. The effects of ageing on selected visual functions: dark adaptation, visual acuity, stereopsis and brightness contrast.SekulerR KlineD DismukesK eds. Ageing and Human Visual Function. 1982;131–159.Liss New York.
OwsleyC, BurtonK. Aging and spatial contrast sensitivity: underlying mechanism and implications for everyday life.BagnoliP HodosW. eds. The Changing Visual System: Maturation and Aging in the Central Nervous System. 1991;119–136.Plenum London.
WealeRA. Senile changes in visual acuity. Trans Ophthalmol Soc UK. 1975;95:36–38.
[PubMed]WealeRA. The eye and the aging. Interdisciplinary Topics in Gerontology. 1978;13:1–13.
WealeRA. Senile ocular changes, cell death, and vision.SekulerR KlineD DismukesK eds. Ageing and Human Visual Function. 1982;161–171.Liss New York.
JayJL, MammoRB, AllanD. Effect of age on visual acuity after cataract extraction. Br J Ophthalmol. 1987;71:112–115.
[CrossRef] [PubMed]CurcioCA, MillicanCL, AllenKA, et al. Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci. 1993;35:783–784.
CurcioCA, DruckerDN. Retinal ganglion cells in Alzheimer’s disease and aging. Ann Neurol. 1993;33:248–257.
[PubMed]OwsleyC, SekulerR, SiemsenD. Contrast sensitivity throughout adulthood. Vision Res. 1983;23:689–699.
[CrossRef] [PubMed]DresslerM, RassowB. Neural contrast sensitivity measurements with a laser interference system for clinical screening application. Invest Ophthalmol Vis Sci. 1981;21:737–744.
[PubMed]KayazawaF, YamamotoT, ItoiM. Clinical measurement of contrast sensitivity function using laser generated sinusoidal grating. Jpn J Ophthalmol. 1981;25:229–236.
WealeRA. Retinal senescence. Prog Retin Res. 1986;5:53–73.
[CrossRef] OrdyMJ, BrizeeKR, JohnsonHA. Cellular alterations in visual pathways and the limbic system: Implications for vision and short-term memory.SekulerR KlineD DismukesK eds. Ageing and Human Visual Function. 1982;79–114.Liss New York.
MorrisonJD, McGrathC. Assessment of the optical contributions to the age-related deterioration in vision. Q J Exp Physiol. 1985;70:249–269.
[CrossRef] [PubMed]OwsleyC, GardnerT, SekulerR, et al. Role of the crystalline lens in the spatial vision loss of the elderly. Invest Ophthalmol Vis Sci. 1985;26:1165–1169.
[PubMed]PorciattiV, BurrDC, MorroneMC, et al. The effects of ageing on the pattern electroretinogram and visual evoked potential in humans. Vision Res. 1992;32:1199–1209.
[CrossRef] [PubMed]BobakP, Bodis-WollnerI, GuilloryS, et al. Aging differentially delays visual evoked potentials to checks and gratings. Clin Vis Sci. 1989;4:269–274.
SokolS, MoskowitzA, TowleVL. Age related changes in latency of the visual evoked potential: Influence of check size. Electroencephalogr Clin Neurophys. 1981;51:559–562.
[CrossRef] TomodaH, CelesiaGG, BrigellMG, et al. The effects of age on steady-state pattern electroretinograms and visual evoked potentials. Doc Ophthalmol. 1991;77:201–211.
[CrossRef] [PubMed]TrickGL, TrickLR, HaywoodKM. Altered pattern evoked retinal and cortical potentials associated with human senescence. Curr Eye Res. 1986;5:717–724.
[CrossRef] [PubMed]SpearPD. Neural bases of visual deficits during aging. Vision Res. 1993;33:2589–2609.
[CrossRef] [PubMed]LevineBK, Beason-HeldLL, PurpuraKP, et al. Age-related differences in visual perception: a PET study. Neurobiol Aging. 2000;21:577–584.
[CrossRef] [PubMed]GradyCL, HaxbyJV, HorwitzB, et al. Dissociation of object and spatial vision in human extrastriate cortex: age-related changes in activation of regional cerebral blood flow measured with [15 O] water and positron emission tomography. J Cogn Neurosci. 1992;4:23–24.
[CrossRef] [PubMed]GradyCL, MaisogJM, HorwitzB, et al. Age-related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci. 1994;14:1450–1462.
[PubMed]GradyCL, McIntoshAR, HorwitzB, et al. Age-related reductions in human recognition memory due to impaired encoding. Science. 1995;269:218–221.
[CrossRef] [PubMed]SnowdenRJ, KavanaghE. Motion perception in the ageing visual system: minimum motion, motion coherence and speed discrimination thresholds. Perception. 2006;35:9–24.
[CrossRef] [PubMed]TanakaK, FukadaY, SaitoHA. Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. J Neurophysiol. 1989;62:642–656.
[PubMed]MorroneMC, TosettiM, MontanaroD, et al. A cortical area that responds specifically to optic flow, revealed by functional magnetic resonance imaging. Nat Neurosci. 2000;3:1322–1328.
[CrossRef] [PubMed]MoutoussisK, ZekiS. Seeing invisible motion: a human FMRI study. Curr Biol. 2006;16:574–579.
[CrossRef] [PubMed]O’BrienHL, TetewskySJ, AveryLM, et al. Visual mechanisms of spatial disorientation in Alzheimer’s disease. Cereb Cortex. 2001;11:1083–1092.
[CrossRef] [PubMed]BettsLR, TaylorCP, SekulerAB, et al. Aging reduces centre-surround antagonism in visual motion processing. Neuron. 2005;45:361–366.
[CrossRef] [PubMed]LeventhalAG, WangY, PuM, et al. GABA and its agonists improved visual cortical function in senescent monkeys. Science. 2003;300:721–722.
TadinD, BlakeR. Motion perception getting better with age. Neuron. 2005;45:325–332.
[CrossRef] [PubMed]HerbertAM, OverburyO, SinghJ, FaubertJ. Aging and bilateral symmetry detection. J Gerontol B Psychol Sci Soc Sci. 2002;57:241–245.
[CrossRef] HabakC, FaubertJ. Larger effect of aging on the perception of higher-order stimuli. Vision Res. 2000;40:943–950.
[CrossRef] [PubMed]FaubertJ. Visual perception and aging. Can J Exp Psychol. 2002;56:164–176.
[CrossRef] [PubMed]FieldDJ, HayesA, HessRF. Contour integration by the human visual system: evidence for a local “association field.”. Vision Res. 1993;33:173–193.
[CrossRef] [PubMed]KovacsI, JuleszB. A closed curve is much more than an incomplete one: effect of closure on figure-ground segmentation. Proc Natl Acad Sci USA. 1993;90:7495–7497.
[CrossRef] [PubMed]KovacsI, JuleszB. Perceptual sensitivity maps within globally defined visual shapes. Nature. 1994;370:644–646.
[CrossRef] [PubMed]LiW, GilbertCD. Global contour saliency and local collinear interactions. J Neurophysiol. 2002;88:2846–2856.
[CrossRef] [PubMed]SaarinenJ, LeviDM, ShenB. Integration of local pattern elements into a global shape in human vision. Proc Natl Acad Sci USA. 1997;94:8267–8271.
[CrossRef] [PubMed]SaarinenJ, LeviDM. Integration of local features into a global shape. Vision Res. 2001;41:1785–1790.
[CrossRef] [PubMed]PolatU, SagiD. Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments. Vision Res. 1993;33:993–999.
[CrossRef] [PubMed]GilbertCD, WieselTN. Morphology and intracortical connections of functionally characterised neurones in the cat visual cortex. Nature. 1979;280:120–125.
[CrossRef] [PubMed]GilbertCD, WieselTN. Clustered intrinsic connections in cat visual cortex. J Neurosci. 1983;3:1116–1133.
[PubMed]GilbertCD, WieselTN. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci. 1989;9:2432–2442.
[PubMed]Ts’oDY, GilbertCD. The organization of chromatic and spatial interactions in the primate striate cortex. J Neurosci. 1988;8:1712–1727.
[PubMed]KapadiaMK, ItoM, GilbertCD, et al. Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron. 1995;15:843–856.
[CrossRef] [PubMed]DasA, GilbertCD. Receptive field expansion in adult visual cortex is linked to changes in strength of cortical connections. J Neurophysiol. 1995;74:779–792.
[PubMed]KovacsI, KozmaP, FeherA, et al. Late maturation of visual spatial integration in humans. Proc Natl Acad Sci USA. 1999;96:12204–12209.
[CrossRef] [PubMed]Del VivaMM, IgliozziR, TancrediR, et al. Spatial and motion integration in children with autism. Vision Res. 2006;46:1242–1252.
[CrossRef] [PubMed]PicciniC, Lauro-GrottoR, Del VivaMM, et al. Agnosia for global patterns: when the cross-talk between grouping and visual selective attention fails. Cogn Neurosci. 2003;20:3–25.
WatsonAB, PelliDG. QUEST. A Bayesian adaptive psychometric method. Percept Psychophys. 1983;33:113–120.
[CrossRef] [PubMed]WeibullWA. A statistical distribution function of wide applicability. J Appl Mechanisms. 1951;18:292–297.
FaubertJ, BellefeuilleA. Aging effects on intra- and inter-attribute spatial frequency information for luminance, color, and working memory. Vision Res. 2002;42:369–378.
[CrossRef] [PubMed]RocklandKS, LundJS. Widespread periodic intrinsic connections in the tree shrew visual cortex. Science. 1982;215:1532–1534.
[CrossRef] [PubMed]MitchisonGJ, CrickF. Long axons within the striate cortex: their distribution, orientation, and patterns of connection. Proc Natl Acad Sci USA. 1982;79:3661–3665.
[CrossRef] [PubMed]NelsonJI, FrostBJ. Intracortical facilitation among co-oriented, co-axially aligned simple cells in cat striate cortex. Exp Brain Res. 1985;61:54–61.
[PubMed]GilbertCD. Adult cortical dynamics. Physiol Rev. 1998;78:467–485.
[PubMed]GilbertCD. Horizontal integration and cortical dynamics. Neuron. 1992;9:1–13.
[CrossRef] [PubMed]FinkGR, HalliganPW, MarshallJC, et al. Where in the brain does visual attention select the forest and the trees?. Nature. 1996;382:626–628.
[CrossRef] [PubMed]HupéJM, JamesAC, PayneBR, et al. Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature. 1998;394:784–787.
[CrossRef] [PubMed]BurkhalterA. Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex. 1993;3:475–487.
WilsonHR, WilkinsonF. Detection of global structure in glass patterns: implication for form vision. Vision Res. 1998;44:2629–2641.
AdamsI, JonesDG. Effects of normal and pathological aging on brain morphology: neurons and synapses. Current Topics in Research on Synapses. 1987;1–84.Liss New York.
Aston-JonesG, RogersJ, ShaverRD, et al. Age-impaired impulse flow from nucleus basalis to cortex. Nature. 1985;318:462–464.
[CrossRef] [PubMed]BarnesCA, FosterTC, RaoG, et al. Specificity of functional changes during normal brain aging. Ann NY Acad Sci. 1991;640:80–85.
[PubMed]ColemanPD, FloodDG. Neuron numbers and dendritic extent in normal aging and Alzheimer’s disease. Neurobiol of Aging. 1987;8:521–545.
[CrossRef] FloodDG, ColemanPD. Neuron numbers and sizes in aging brain: comparison of human, monkey, and rodent data. Neurobiol of Aging. 1988;9:453–464.
[CrossRef] SeversonJA. Synaptic regulation of neurotransmitter function in aging. Rev Biol Res into Aging. 1987;3:191–206.
LynchJJ, SilveiraLC, PerryVH, et al. Visual effects of damage to P-ganglion cells in macaques. Vis Neurosci. 1992;8:575–583.
[CrossRef] [PubMed]MeriganWH, KatzLM, MaunsellJH. The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. J Neurosci. 1991;11:994–1001.
[PubMed]ConnorJR, Jr, DiamondMC, JohnsonRE. Aging and environmental influences on two types of dendritic spines in the rat occipital cortex. Exp Neurol. 1980;70:371–379.
[CrossRef] [PubMed]LeubaG. Aging of dendrites in the cerebral cortex of the mouse. Neuropathol Appl Neurol. 1983;9:467–475.
[CrossRef] PetersA, MossMB, SetharesC. The effects of aging on layer 1 of primary visual cortex in the Rhesus Monkey. Cereb Cortex. 2001;11:93–103.
[CrossRef] [PubMed]YuaS, WangaY, LiaX, ZhouaY, LeventhalAG. Functional degradation of extrastriate visual cortex in senescent rhesus monkeys. Neuroscience. 2006;140:1023–1029.
[CrossRef] [PubMed]