Abstract
The modular layout of striate cortex is arguably a hallmark of all cortical organization. Neurons of a given module or domain respond optimally to very few specific properties, such as orientation or direction. However, it is possible, under appropriate conditions, to compel a neuron to respond preferentially to a different optimal property. In anesthetized cats, prepared for electrophysiological recordings in the visual cortex, we applied a spatial frequency (SF) that differs (by 0.25–3.0 octaves) from the optimal one for 7–13 min without interruption. This application shifted the tuning curve of the cell mainly in the direction of the imposed SF. Indeed, results indicate an attractive push occurring more frequently (50%) than a repulsive (30%) shift in cortical cells. The increase of responsivity is band-limited and is around the imposed SF, while flanked responses remained unmodified in all conditions. We hypothesize that the observed reversible plasticity is obtained by a modulation of the balance between the strengths of the respective synaptic inputs. These changes in preferred original optimal spatial frequencies may allow a dynamic reaction of cortex to a new environment and particularly to ‘‘zoom’’ cellular activity toward persistent stimuli in spite of the tuning inherited from genetic programming of response properties and environmental conditions during critical periods in new born animals.
Similar content being viewed by others
References
Bardy C, Huang JY, Wang C, Fitzgibbon T, Dreher B (2006) ‘‘Simplification’’ of responses of complex cells in cat striate cortex: suppressive surrounds and feedback inactivation. J Physiol (Lond) 574:731–750
Barlow HB, Földiák P (1989) Adaptation and decorrelation in the cortex. In: Durbin R, Miali C, Mitchinson G (eds) The computing neuron. Addison-Wesley, New York, pp 54–72
Basole A, White LE, Fitzpatrick D (2003) Mapping multiple features in the population response of visual cortex. Nature 423:986–990
Blakemore C, Nachmias J, Sutton P (1970) The perceived spatial frequency shift: evidence for frequency selective neurones in the human brain. J Physiol (Lond) 210:727–750
Carandini M, Ferster DA (1997) A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276:949–952
Chander D, Chichilnisky EJ (2001) Adaptation to temporal contrast in primate and salamander retina. J Neurosci 15:9904–9916
Clifford CW (2002) Perceptual adaptation: motion parallels orientation. Trends Cogn Sci 6:136–143
Das A (2005) Cortical maps: where theory meets experiments. Neuron 47:168–171
De Valois RL, De Valois KK (1990) Multiple spatial frequency channels. In: Broadbent DE, McGaugh JL, Mackintosh NJ, Posner MI, Tulving E, Weiskrantz L (eds) Spatial vision. Oxford Psychology Series. Oxford University Press, Clarendon Press, New York, Oxford, pp 176–211
Dragoi V, Rivadulla C, Sur M (2001) Foci of orientation plasticity tuning in visual cortex. Nature 411:80–86
Dragoi V, Sharma J, Miller EK, Sur M (2002) Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat Neurosci 5:883–891
Dragoi V, Sharma J, Sur M (2000) Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28:287–298
Everson RM, Prashanth AK, Gabbay M, Knight BW, Sirovich L, Kaplan E (1998) Representation of spatial frequency and orientation in the visual cortex. Proc Natl Acad Sci USA 95:8334–8338
Ghisovan N, Nemri A, Shumikhina S, Molotchnikoff S (2007a) Neuronal plasticity in cat primary visual cortex: a neuronal correlate of memory. Perception 36:S33
Ghisovan N, Nemri A, Shumikhina S, Molotchnikoff S (2007b) Cortical cells in area 17 “remember” the adapting orientation applied previously. Society for Neuroscience, Neuroscience Abstracts 920:21
Godde B, Leonhardt R, Cords SM, Dinse HR (2002) Plasticity of orientation preference maps in the visual cortex of adult cats. Proc Natl Acad Sci USA 99:6352–6357
Godde B, Stauffenberg B, Spengler F, Dinse HR (2000) Tactile coactivation-induced changes in spatial discrimination performance. J Neurosci 20:1597–1604
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol (Lond) 160:106–154
Issa NP, Trepel C, Stryker MP (2000) Spatial frequency maps in cat visual cortex. J Neurosci 20:8504–8514
Kohn A, Movshon JA (2003) Neuronal adaptation to visual motion in area MT of the macaque. Neuron 39:681–691
Kohn A, Movshon JA (2004) Adaptation changes the direction tuning of macaque MT neurons. Nat Neurosci 7:764–772
Kohn A (2007) Visual adaptation: physiology, mechanisms, and functional benefits. J Neurophysiol 97:3155–3164
Krekelberg B, van Wezel RJA, Albright TD (2006) Adaptation in macaque MT reduces perceived speed and improves speed discrimination. J Neurophysiol 95:255–270
Levinson E, Sekuler R (1976) Adaptation alters perceived direction of motion. Vis Res 16:779–781
Maunsell JH, Van Essen DC (1983) Functional properties of neurons in the middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed and orientation. J Neurophysiol 49:1127–1147
Milleret C, Buisseret P, Gary-Bobo E (1988) Area centralis position relative to the optic disc projection in kittens as a function of age. Invest Ophthalmol Vis Sci 29:1299–1305
Molotchnikoff S, Gillet P-C, Shumikhina S, Bouchard M (2007) Spatial frequency characteristics of nearbyneurons in cat’s visual cortex. Neurosci Lett 418:242–247
Movshon JA, Lennie P (1979) Pattern-selective adaptation in visual cortical neurones. Nature 278:850–852
Movshon J, Thompson I, Tolhurst D (1978) Receptive field organization of complex cells in the cat’s striate cortex. J Physiol (Lond) 283:79–99
Reinoso-Suarez F (1961) Topographischer Hirnatlas der Katze, Herausgegeben von E. Merck A.G., Darmstadt
Saul AB, Cynader MS (1989a) Adaptation in single units in visual cortex: the tuning of aftereffects in the spatial domain. Vis Neurosci 2:593–607
Saul AB, Cynader MS (1989b) Adaptation in single units in visual cortex: the tuning of aftereffects in the temporal domain. Vis Neurosci 2:609–620
Shou T, Li X, Zhou Y, Hu B (1996) Adaptation of visual evoked responses of relay cells in the dorsal lateral geniculate nucleus of the cat following prolonged exposure to drifting gratings. Vis Neurosci 13:605–613
Sirovich L, Uglesich R (2004) The organization of orientation and spatial frequency in primary visual cortex. Proc Natl Acad Sci USA 101:16941–16946
Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M (1997) Adaptation of retinal processing to image contrast and spatial scale. Nature 386:69–73
Solomon SG, Peirce JW, Dhruv NT, Lennie P (2004) Profound contrast adaptation early in the visual pathway. Neuron 42:155–162
Sur M, Schummers J, Dragoi V (2002) Cortical plasticity: time for a change. Curr Biol 12:R168–R170
Schuett S, Bonhoeffer T, Hübener M (2001) Pairing-induced changes of orientation maps in cat visual cortex. Neuron 32:325–337
Teich AF, Qian N (2003) Learning and adaptation in a recurrent model of V1 orientation selectivity. J Neurophysiol 89:2086–2100
Tolias AS, Keliris GA, Smirnakis SM, Logothetis NK (2005) Neurons in macaque area V4 acquire directional tuning after adaptation to motion stimuli. Nat Neurosci 8:591–593
Vakkur GJ (1963) Visual optics in the cat, including posterior nodal distance and retinal landmarks. Vis Res 61:289–314
Wainwright MJ (1999) Visual adaptation as optimal information transmission. Vis Res 39:3960–3974
Acknowledgments
The authors thank Drs. M. Anctil and S. Itaya for insightful comments. The research is supported by NSERC Canada.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bouchard, M., Gillet, PC., Shumikhina, S. et al. Adaptation changes the spatial frequency tuning of adult cat visual cortex neurons. Exp Brain Res 188, 289–303 (2008). https://doi.org/10.1007/s00221-008-1362-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-008-1362-4