The Role of Thalamic Population Synchrony in the Emergence of Cortical Feature Selectivity

• Type of Material: Article
• Authors: Sean T. Kelly, Emory University; Jens Kremkow, State University of New York; Jianzhong Jin, State University of New York; Yushi Wang, State University of New York; Qi Wang, Columbia University; Jose-Manuel Alonso, State University of New York; Garrett Stanley, Emory University
• Language: English
• Date: 2014-01-09
• Publisher: Public Library of Science
• Publication Version: Final Published Version
• Copyright Statement: © 2014 Kelly et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1371/journal.pcbi.1003418
• Title of Journal or Parent Work: PLoS Computational Biology
• ISSN: 1553-734X
• Volume: 10
• Issue: 1
• Start Page: e1003418
• End Page: e1003418
• Grant/Funding Information: Funding by: NIH EY005253, NIH NS48285, NSF CRCNS IIS-0904630 (http://www.nsf.gov/funding/pgm_summ.jsp?pims_id=5147) and DFG Research Fellowship (JK).
• Keywords: Biochemistry & Molecular Biology; SOMATOSENSORY CORTEX; Biochemical Research Methods; Life Sciences & Biomedicine; SIMPLE CELLS; BIOCHEMICAL RESEARCH METHODS; RESPONSE VARIABILITY; ORIENTATION SELECTIVITY; PRIMARY VISUAL-CORTEX; RECEPTIVE-FIELDS; LATERAL GENICULATE-NUCLEUS; COINCIDENCE DETECTION; Mathematical & Computational Biology; MATHEMATICAL & COMPUTATIONAL BIOLOGY; SINGLE NEURONS; Science & Technology; TIMING PRECISION
• Research Categories: Engineering, Biomedical

Abstract

In a wide range of studies, the emergence of orientation selectivity in primary visual cortex has been attributed to a complex interaction between feed-forward thalamic input and inhibitory mechanisms at the level of cortex. Although it is well known that layer 4 cortical neurons are highly sensitive to the timing of thalamic inputs, the role of the stimulus-driven timing of thalamic inputs in cortical orientation selectivity is not well understood. Here we show that the synchronization of thalamic firing contributes directly to the orientation tuned responses of primary visual cortex in a way that optimizes the stimulus information per cortical spike. From the recorded responses of geniculate X-cells in the anesthetized cat, we synthesized thalamic sub-populations that would likely serve as the synaptic input to a common layer 4 cortical neuron based on anatomical constra ints. We used this synchronized input as the driving input to an integrate-and-fire model of cortical responses and demonstrated that the tuning properties match closely to those measured in primary visual cortex. By modulating the overall level of synchronization at the preferred orientation, we show that efficiency of information transmission in the cortex is maximized for levels of synchronization which match those reported in thalamic recordings in response to naturalistic stimuli, a property which is relatively invariant to the orientation tuning width. These findings indicate evidence for a more prominent role of the feed-forward thalamic input in cortical feature selectivity based on thalamic synchronization.