The role of high-level visual areas in short- and longer-lasting forms of neural plasticity

Striate and extrastriate neurons present short-term synaptic depression and facilitation in response to brief stimulations. Recent psychophysical studies have shed light on some possible relationships between these short-term forms of neural plasticity and of psychophysical behavior. It has been shown that a brief adaptation to directional motion biases the perceived direction of a subsequently presented ambiguous test pattern towards the same direction to that of the adaptation (rapid visual motion priming--rVMP), but only after brief (40ms) adaptation-test blank intervals. Although when the adaptation duration is increased, the perceived motion direction of the ambiguous test pattern is biased towards the opposite direction to that of the adaptation pattern (rapid motion aftereffect--rMAE). In the present study we stimulated MT and MST neurons via the presentation of contracting and expanding circular gratings. Our aim was to assess whether rapid effects exist at these higher levels of processing where neurons respond to optic flow, and if such effects are present determine their timescale. Results revealed strong rMAEs and perceptual sensitization (PS), which is a long-lasting facilitation that increases gradually when using intermediate and long adaptation-test blank intervals. We did not observe any effect of rVMP. Our results are considered to reflect the competition between coexistent forms of short- and long-term synaptic depression and facilitation implemented at different visual cortical circuitries.

[1]  Gianluca Campana,et al.  Priming of motion direction and area V5/MT: a test of perceptual memory. , 2002, Cerebral cortex.

[2]  G. Campana,et al.  The principle of good continuation in space and time can guide visual search in absence of priming or contextual cueing , 2007 .

[3]  M. Graziano,et al.  Tuning of MST neurons to spiral motions , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  S. Nelson,et al.  Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. , 2000, Journal of neurophysiology.

[5]  G. Campana,et al.  Separate motion-detecting mechanisms for first- and second-order patterns revealed by rapid forms of visual motion priming and motion aftereffect. , 2009, Journal of vision.

[6]  G. Campana,et al.  Where perception meets memory: A review of repetition priming in visual search tasks , 2010, Attention, perception & psychophysics.

[7]  H. Pashler,et al.  Repetition priming in visual search: Episodic retrieval, not feature priming , 2004, Memory & cognition.

[8]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[9]  Maninder K. Kahlon,et al.  Visual Motion Analysis for Pursuit Eye Movements in Area MT of Macaque Monkeys , 1999, The Journal of Neuroscience.

[10]  T. Ledgeway Adaptation to second-order motion results in a motion aftereffect for directionally-ambiguous test stimuli , 1994, Vision Research.

[11]  J J Jack,et al.  Synaptic interactions between smooth and spiny neurones in layer 4 of cat visual cortex in vitro , 1998, The Journal of physiology.

[12]  A. T. Smith,et al.  Sensitivity to optic flow in human cortical areas MT and MST , 2006, The European journal of neuroscience.

[13]  P. Somogyi,et al.  Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. , 1997, The Journal of physiology.

[14]  Juha Silvanto,et al.  Contrasting early visual cortical activation states causally involved in visual imagery and short‐term memory , 2009, The European journal of neuroscience.

[15]  Mazyar Fallah,et al.  Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions , 2003, Neuropsychologia.

[16]  Emad N Eskandar,et al.  Parietal activity and the perceived direction of ambiguous apparent motion , 2003, Nature Neuroscience.

[17]  David A. Leopold,et al.  Stable perception of visually ambiguous patterns , 2002, Nature Neuroscience.

[18]  Nicholas J. Priebe,et al.  Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex , 2005, The Journal of Neuroscience.

[19]  J. Deuchars,et al.  Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. , 1996, The Journal of physiology.

[20]  J. A. Varela,et al.  Differential Depression at Excitatory and Inhibitory Synapses in Visual Cortex , 1999, The Journal of Neuroscience.

[21]  K. Magleby,et al.  Augmentation and facilitation of transmitter release. A quantitative description at the frog neuromuscular junction , 1982, The Journal of general physiology.

[22]  Á. Kristjánsson,et al.  Priming of luminance-defined motion direction in visual search , 2009 .

[23]  S. Nelson,et al.  Temporal interactions in the cat visual system. III. Pharmacological studies of cortical suppression suggest a presynaptic mechanism , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  P Cavanagh,et al.  Attention-based motion perception. , 1992, Science.

[25]  Gianluca Campana,et al.  Repetition effects of features and spatial position: evidence for dissociable mechanisms. , 2009, Spatial vision.

[26]  Juha Silvanto,et al.  Transcranial magnetic stimulation reveals the content of visual short-term memory in the visual cortex , 2010, NeuroImage.

[27]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[28]  Nicholas J. Priebe,et al.  Constraints on the source of short-term motion adaptation in macaque area MT. I. the role of input and intrinsic mechanisms. , 2002, Journal of Neurophysiology.

[29]  Á. Kristjánsson,et al.  Object- and feature-based priming in visual search , 2008, Psychonomic bulletin & review.

[30]  T. Shallice,et al.  Neuroimaging evidence for dissociable forms of repetition priming. , 2000, Science.

[31]  E. Macaluso,et al.  Neural basis for priming of pop-out during visual search revealed with fMRI. , 2007, Cerebral cortex.

[32]  G. Campana,et al.  Priming of first- and second-order motion: Mechanisms and neural substrates , 2008, Neuropsychologia.

[33]  Gianluca Campana,et al.  Visual area V5/MT remembers "what" but not "where". , 2004, Cerebral cortex.

[34]  L. Abbott,et al.  A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex , 1997, The Journal of Neuroscience.

[35]  D. Burr,et al.  Temporal integration of optic flow, measured by contrast and coherence thresholds , 2001, Vision Research.

[36]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[37]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[38]  B. Connors,et al.  Short-term synaptic enhancement and long-term potentiation in neocortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[39]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[40]  Ning Qian,et al.  The effect of complex motion pattern on speed perception , 1998, Vision Research.

[41]  J. Maunsell,et al.  Attentional Modulation of Behavioral Performance and Neuronal Responses in Middle Temporal and Ventral Intraparietal Areas of Macaque Monkey , 2002, The Journal of Neuroscience.

[42]  Frans A. J. Verstraten,et al.  Perceptual manifestations of fast neural plasticity: Motion priming, rapid motion aftereffect and perceptual sensitization , 2005, Vision Research.

[43]  P. Cavanagh,et al.  Looking ahead: the perceived direction of gaze shifts before the eyes move. , 2009, Journal of vision.

[44]  Karl J. Friston,et al.  How the brain learns to see objects and faces in an impoverished context , 1997, Nature.

[45]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[46]  Gianluca Campana,et al.  Left frontal eye field remembers “where” but not “what” , 2007, Neuropsychologia.

[47]  D. Burr,et al.  A cortical area that responds specifically to optic flow, revealed by fMRI , 2000, Nature Neuroscience.

[48]  Sheng He,et al.  Local Factors Determine the Stabilization of Monocular Ambiguous and Binocular Rivalry Stimuli , 2004, Current Biology.

[49]  A. M. Derrington,et al.  Slow discrimination of contrast-defined expansion patterns , 2000, Vision Research.

[50]  D. Burr,et al.  Large receptive fields for optic flow detection in humans , 1998, Vision Research.

[51]  G. Mather,et al.  The motion aftereffect reloaded , 2008, Trends in Cognitive Sciences.

[52]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[53]  Frances S. Chance,et al.  Synaptic Depression and the Temporal Response Characteristics of V1 Cells , 1998, The Journal of Neuroscience.

[54]  L. Vaina Complex motion perception and its deficits , 1998, Current Opinion in Neurobiology.

[55]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[56]  M. Cynader,et al.  Synaptic depression in visual cortex tissue slices: an in vitro model for cortical neuron adaptation , 2004, Experimental Brain Research.

[57]  A. Pinkus,et al.  Probing Visual Motion Signals with a Priming Paradigm , 1997, Vision Research.

[58]  N. Logothetis,et al.  Multistable phenomena: changing views in perception , 1999, Trends in Cognitive Sciences.

[59]  Angelika Lingnau,et al.  Selective visual responses to expansion and rotation in the human MT complex revealed by functional magnetic resonance imaging adaptation , 2008, The European journal of neuroscience.

[60]  D. Burr,et al.  Two stages of visual processing for radial and circular motion , 1995, Nature.

[61]  J. Maunsell,et al.  Effects of Attention on the Processing of Motion in Macaque Middle Temporal and Medial Superior Temporal Visual Cortical Areas , 1999, The Journal of Neuroscience.

[62]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

[63]  A. Thomson Activity‐dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro , 1997, The Journal of physiology.

[64]  Alexander Maier,et al.  Perception of Temporally Interleaved Ambiguous Patterns , 2003, Current Biology.