Effects of electrical coupling among layer 4 inhibitory interneurons on contrast-invariant orientation tuning

Simulations of orientation selectivity in visual cortex have shown that layer 4 complex cells lacking orientation tuning are ideal for providing global inhibition that scales with contrast in order to produce simple cells with contrast-invariant orientation tuning (Lauritzen and Miller in J Neurosci 23:10201-10213, 2003). Inhibitory cortical cells have been shown to be electrically coupled by gap junctions (Fukuda and Kosaka in J Neurosci 120:5-20, 2003). Such coupling promotes, among other effects, spike synchronization and coordination of postsynaptic IPSPs (Beierlein et al. in Nat Neurosci 3:904-910, 2000; Galarreta and Hestrin in Nat Rev Neurosci 2:425-433, 2001). Consequently, it was expected (Miller in Cereb Cortex 13:73-82, 2003) that electrical coupling would promote nonspecific functional responses consistent with the complex inhibitory cells seen in layer 4 which provide broad inhibition in response to stimuli of all orientations (Miller et al. in Curr Opin Neurobiol 11:488-497, 2001). This was tested using a mechanistic modeling approach. The orientation selectivity model of Lauritzen and Miller (J Neurosci 23:10201-10213, 2003) was reproduced with and without electrical coupling between complex inhibitory neurons. Although extensive coupling promotes uniform firing in complex cells, there were no detectable improvements in contrast-invariant orientation selectivity unless there were coincident changes in complex cell firing rates to offset the untuned excitatory component that grows with contrast. Thus, changes in firing rates alone (with or without coupling) could improve contrast-invariant orientation tuning of simple cells but not synchronization of complex inhibitory neurons alone.