A homeostatic rule for inhibitory synapses promotes temporal sharpening and cortical reorganization

Experience with transient stimuli leads to stronger neural responses that also rise and fall more sharply in time. This sharpening enhances the processing of transients and may be especially relevant for speech perception. We consider a learning rule for inhibitory connections that promotes this sharpening effect by adjusting these connections to maintain a target homeostatic level of activity in excitatory neurons. We analyze this rule in a recurrent network model of excitatory and inhibitory units. Strengthening inhibitory→excitatory connections along with excitatory→excitatory connections is required to obtain a sharpening effect. Using the homeostatic rule, we show that repeated presentations of a transient signal will “teach” the network to respond to the signal with both higher amplitude and shorter duration. The model also captures reorganization of receptive fields in the sensory hand area after amputation or peripheral nerve resection.

[1]  Heinz Zemanek,et al.  Kybernetik , 1964, Elektron. Rechenanlagen.

[2]  H. Robinson,et al.  Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. , 2004, Journal of neurophysiology.

[3]  D. Simons,et al.  Circuit dynamics and coding strategies in rodent somatosensory cortex. , 2000, Journal of neurophysiology.

[4]  Daniel E Feldman,et al.  Synaptic basis for developmental plasticity in somatosensory cortex , 2004, Current Opinion in Neurobiology.

[5]  D. Rasmusson,et al.  Immediate effects of digit amputation on SI cortex in the raccoon: unmasking of inhibitory fields , 1983, Brain Research.

[6]  Liisa A. Tremere,et al.  Role of inhibition in cortical reorganization of the adult raccoon revealed by microiontophoretic blockade of GABA(A) receptors. , 2001, Journal of neurophysiology.

[7]  Michael M Merzenich,et al.  Local circuit properties underlying cortical reorganization. , 2002, Journal of neurophysiology.

[8]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[9]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  C. Gilbert,et al.  Long‐term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex. , 1993, The Journal of physiology.

[11]  G. Recanzone,et al.  Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task. , 1992, Journal of neurophysiology.

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

[13]  Karel Svoboda,et al.  Circuit Analysis of Experience-Dependent Plasticity in the Developing Rat Barrel Cortex , 2003, Neuron.

[14]  Kenneth D Miller,et al.  Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex , 2001, Current Opinion in Neurobiology.

[15]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[16]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[17]  M. Stryker,et al.  Local GABA circuit control of experience-dependent plasticity in developing visual cortex. , 1998, Science.

[18]  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.

[19]  J. Cowan,et al.  A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue , 1973, Kybernetik.

[20]  W M Jenkins,et al.  Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. , 1992, Journal of neurophysiology.

[21]  B. Connors,et al.  Sensory experience modifies the short-term dynamics of neocortical synapses , 1999, Nature.

[22]  R. Siegler,et al.  Mechanisms of cognitive development. , 1989, Annual review of psychology.

[23]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[24]  Bard Ermentrout,et al.  Simulating, analyzing, and animating dynamical systems - a guide to XPPAUT for researchers and students , 2002, Software, environments, tools.

[25]  D. Rasmusson,et al.  Reorganization of raccoon somatosensory cortex following removal of the fifth digit , 1982, The Journal of comparative neurology.

[26]  K. Fox,et al.  Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex , 2002, Neuroscience.

[27]  Malgorzata Kossut,et al.  Long‐term depression and long‐term potentiation in horizontal connections of the barrel cortex , 2002, The European journal of neuroscience.

[28]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[29]  P. Tallal,et al.  Defects of Non-Verbal Auditory Perception in Children with Developmental Aphasia , 1973, Nature.

[30]  E. Oja.  Simplified neuron model as a principal component analyzer , 1982, Journal of mathematical biology.

[31]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.