Functional interactions among neurons in inferior temporal cortex of the awake macaque

SummaryFunctional interactions among inferior temporal cortex (IT) neurons were studied in the awake, fixating macaque monkey during the presentation of visual stimuli. Extracellular recordings were obtained simultaneously from several microelectrodes, and in many cases, spike trains from more than one neuron were extracted from each electrode by the use of spike shape sorting technology. Functional interactions between pairs of neurons were measured using cross-correlation. Discharge patterns of single neurons were evaluated using auto-correlation and PST histograms. Neurons recorded on the same electrode (within about 100 μn) had more similar stimulus selectivity and were more likely to show functional interactions than those recorded on different electrodes spaced about 250 to 500 microns apart. Most neurons tended to fire in bursts tens to hundreds of milliseconds in duration, and asynchronously from the stimulus induced rate changes. Correlated neuronal firing indicative of shared inputs and direct interactions was observed. Occurrence of shared input was significantly lower for neuron pairs recorded on different electrodes than for neurons recorded on the same electrode. Direct connections occurred about as often for neurons on different electrodes as for neurons on the same electrode. These results suggest that input projections are usually restricted to less than 500 μm patches and are then distributed over greater distances by intrinsic connections. Measurements of synaptic contribution suggest that typically more than 5 near-simultaneous inputs are required to cause an IT neuron to discharge.

[1]  D. Ts'o,et al.  The organization of chromatic and spatial interactions in the primate striate cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  George L. Gerstein,et al.  Design of a laboratory for multineuron studies , 1983, IEEE Transactions on Systems, Man, and Cybernetics.

[3]  D. B. Bender,et al.  Activity of inferior temporal neurons in behaving monkeys , 1979, Neuropsychologia.

[4]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[5]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[6]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[7]  J. Krüger,et al.  Multimicroelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers. , 1988, Journal of neurophysiology.

[8]  Stephen Grossberg,et al.  Competitive Learning: From Interactive Activation to Adaptive Resonance , 1987, Cogn. Sci..

[9]  E. Fetz,et al.  Intracortical connectivity revealed by spike-triggered averaging in slice preparations of cat visual cortex , 1988, Brain Research.

[10]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[11]  O. D. Creutzfeldt,et al.  Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat , 1978, Experimental Brain Research.

[12]  C. Gross Visual Functions of Inferotemporal Cortex , 1973 .

[13]  C. Gross 7 – The Neural Basis of Stimulus Equivalence Across Retinal Translation , 1977 .

[14]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[15]  M. Abeles Local Cortical Circuits: An Electrophysiological Study , 1982 .

[16]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[17]  H. L. Bryant,et al.  Correlations of neuronal spike discharges produced by monosynaptic connections and by common inputs. , 1973, Journal of neurophysiology.

[18]  C. Legéndy,et al.  Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. , 1985, Journal of neurophysiology.

[19]  R. Desimone,et al.  Visual areas in the temporal cortex of the macaque , 1979, Brain Research.

[20]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Abeles Quantification, smoothing, and confidence limits for single-units' histograms , 1982, Journal of Neuroscience Methods.

[22]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  G. L. Gerstein,et al.  Interactions between cat striate cortex neurons , 2004, Experimental Brain Research.

[24]  M. Ito,et al.  Functional synaptic organization of primary visual cortex neurones in the cat , 2004, Experimental Brain Research.

[25]  K. Tanaka,et al.  Cross-Correlation Analysis of Interneuronal Connectivity in cat visual cortex. , 1981, Journal of neurophysiology.

[26]  H. Tamura,et al.  Inhibition contributes to orientation selectivity in visual cortex of cat , 1988, Nature.

[27]  George L. Gerstein,et al.  Coordinated activity of neuron pairs in anesthetized rat dorsal cochlear nucleus , 1989, Brain Research.

[28]  E. Rolls,et al.  Functional subdivisions of the temporal lobe neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  A. Aertsen,et al.  Evaluation of neuronal connectivity: Sensitivity of cross-correlation , 1985, Brain Research.

[30]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. F. Sarna,et al.  Unsupervised waveform classification for multi-neuron recordings: a real-time, software-based system. II. Performance comparison to other sorters , 1988, Journal of Neuroscience Methods.

[32]  M. Abeles,et al.  Multispike train analysis , 1977, Proceedings of the IEEE.

[33]  W. Levick,et al.  Lateral geniculate neurons of cat: retinal inputs and physiology. , 1972, Investigative ophthalmology.

[34]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[35]  Ad Aertsen,et al.  Dynamics of Activity in Neuronal Networks Give Rise to Fast Modulations of Functional Connectivity , 1990 .

[36]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[37]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  P. M. Gochin,et al.  A hierarchical machine vision system based on a model of the primate visual system , 1990, Proceedings. 5th IEEE International Symposium on Intelligent Control 1990.

[39]  V. Mountcastle,et al.  Response properties of neurons of cat's somatic sensory cortex to peripheral stimuli. , 1957, Journal of neurophysiology.

[40]  D. Mastronarde Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. , 1983, Journal of neurophysiology.

[41]  A. Aertsen,et al.  Neuronal assemblies , 1989, IEEE Transactions on Biomedical Engineering.