Activity Recall in Visual Cortical Ensemble

Cue-triggered recall of learned temporal sequences is an important cognitive function that has been attributed to higher brain areas. Here recordings in both anesthetized and awake rats demonstrate that after repeated stimulation with a moving spot that evoked sequential firing of an ensemble of primary visual cortex (V1) neurons, just a brief flash at the starting point of the motion path was sufficient to evoke a sequential firing pattern that reproduced the activation order evoked by the moving spot. The speed of recalled spike sequences may reflect the internal dynamics of the network rather than the motion speed. In awake rats, such recall was observed during a synchronized ('quiet wakeful') brain state having large-amplitude, low-frequency local field potential (LFP) but not in a desynchronized ('active') state having low-amplitude, high-frequency LFP. Such conditioning-enhanced, cue-evoked sequential spiking of a V1 ensemble may contribute to experience-based perceptual inference in a brain state–dependent manner.

[1]  A. Hughes,et al.  A schematic eye for the rat , 1979, Vision Research.

[2]  A. Fiorentini,et al.  Perceptual learning specific for orientation and spatial frequency , 1980, Nature.

[3]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[4]  K D Miller,et al.  Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[5]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[7]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[8]  M. Ahissar,et al.  Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. , 1992, Science.

[9]  R. Metherate,et al.  Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex , 1993, Synapse.

[10]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[12]  R P Kesner,et al.  Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. , 1994, Behavioral and neural biology.

[13]  K. I. Blum,et al.  Functional significance of long-term potentiation for sequence learning and prediction. , 1996, Cerebral cortex.

[14]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[15]  R. G. Morris.  D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949 , 1999, Brain Research Bulletin.

[16]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[17]  J. Csicsvari,et al.  Replay and Time Compression of Recurring Spike Sequences in the Hippocampus , 1999, The Journal of Neuroscience.

[18]  T. Tsumoto,et al.  Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input , 1999, The European journal of neuroscience.

[19]  Rajesh P. N. Rao,et al.  Predictive Sequence Learning in Recurrent Neocortical Circuits , 1999, NIPS.

[20]  E. Ahissar,et al.  A neuronal analogue of state-dependent learning , 2000, Nature.

[21]  Y. Dan,et al.  Stimulus Timing-Dependent Plasticity in Cortical Processing of Orientation , 2001, Neuron.

[22]  E. Ahissar,et al.  Acetylcholine-dependent induction and expression of functional plasticity in the barrel cortex of the adult rat. , 2001, Journal of neurophysiology.

[23]  G. Orban,et al.  Practising orientation identification improves orientation coding in V1 neurons , 2001, Nature.

[24]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[25]  Y. Dan,et al.  Temporal Specificity in the Cortical Plasticity of Visual Space Representation , 2002, Science.

[26]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[27]  Paul E. Gilbert,et al.  The role of the hippocampus in memory for the temporal order of a sequence of odors. , 2002, Behavioral neuroscience.

[28]  M. Lavine,et al.  Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas , 2004, PLoS biology.

[29]  C. Furmanski,et al.  Learning Strengthens the Response of Primary Visual Cortex to Simple Patterns , 2004, Current Biology.

[30]  M. Nicolelis,et al.  Global Forebrain Dynamics Predict Rat Behavioral States and Their Transitions , 2004, The Journal of Neuroscience.

[31]  C. Gilbert,et al.  Perceptual learning and top-down influences in primary visual cortex , 2004, Nature Neuroscience.

[32]  A. Yuille,et al.  Object perception as Bayesian inference. , 2004, Annual review of psychology.

[33]  Amiram Grinvald,et al.  VSDI: a new era in functional imaging of cortical dynamics , 2004, Nature Reviews Neuroscience.

[34]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

[35]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  Y. Dan,et al.  Contribution of individual spikes in burst-induced long-term synaptic modification. , 2006, Journal of neurophysiology.

[37]  C. Petersen,et al.  Correlating whisker behavior with membrane potential in barrel cortex of awake mice , 2006, Nature Neuroscience.

[38]  J. Alonso,et al.  Thalamic Burst Mode and Inattention in the Awake LGNd , 2006, Neuron.

[39]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[40]  D. R. Euston,et al.  Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep , 2007, Science.

[41]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[42]  Feng Qi Han,et al.  Reverberation of Recent Visual Experience in Spontaneous Cortical Waves , 2008, Neuron.

[43]  I. Fried,et al.  Internally Generated Reactivation of Single Neurons in Human Hippocampus During Free Recall , 2008, Science.

[44]  J. Poulet,et al.  Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice , 2008, Nature.

[45]  J. O’Neill,et al.  Reactivation of experience-dependent cell assembly patterns in the hippocampus , 2008, Nature Neuroscience.

[46]  A D Redish,et al.  Prediction, sequences and the hippocampus , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  M. Witter,et al.  A Specific Role of the Human Hippocampus in Recall of Temporal Sequences , 2009, The Journal of Neuroscience.

[48]  Mattias P. Karlsson,et al.  Awake replay of remote experiences in the hippocampus , 2009, Nature Neuroscience.

[49]  Matthew A. Wilson,et al.  Hippocampal Replay of Extended Experience , 2009, Neuron.

[50]  R. Buckner.  The role of the hippocampus in prediction and imagination. , 2010, Annual review of psychology.

[51]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.