Contrast Dependence and Differential Contributions from Somatostatin- and Parvalbumin-Expressing Neurons to Spatial Integration in Mouse V1

Abstract

A characteristic feature in the primary visual cortex is that visual responses are suppressed as a stimulus extends beyond the classical receptive field. Here, we examined the role of inhibitory neurons expressing somatostatin (SOM ϩ ) or parvalbumin (PV ϩ ) on surround suppression and preferred receptive field size. We recorded multichannel extracellular activity in V1 of transgenic mice expressing channelrhodopsin in SOM ϩ neurons or PV ϩ neurons. Preferred size and surround suppression were measured using drifting squarewave gratings of varying radii and at two contrasts. Consistent with findings in primates, we found that the preferred size was larger for lower contrasts across all cortical depths, whereas the suppression index (SI) showed a trend to decrease with contrast. We then examined the effect of these metrics on units that were suppressed by photoactivation of either SOM ϩ or PV ϩ neurons. When activating SOM ϩ neurons, we found a significant increase in SI at cortical depths Ͼ400 m, whereas activating PV ϩ neurons caused a trend toward lower SIs regardless of cortical depth. Conversely, activating PV ϩ neurons significantly increased preferred size across all cortical depths, similar to lowering contrast, whereas activating SOM ϩ neurons had no systematic effect on preferred size across all depths. These data suggest that SOM ϩ and PV ϩ neurons contribute differently to spatial integration. Our findings are compatible with the notion that SOM ϩ neurons mediate surround suppression, particularly in deeper cortex, whereas PV ϩ activation decreases the drive of the input to cortex and therefore resembles the effects on spatial integration of lowering contrast.

Spatial integration in mouse primary visual cortex

“…Increasing PVϩ activity likely reduces stimulus drive by controlling the overall responsiveness in the network. Indeed, our observed effects of PVϩ interneuron activation on spatial integration are similar to those obtained when stimulus contrast is lowered (see also Nienborg et al 2013). Consistent with a general modulation of stimulus drive, PVϩ interneurons have recently been implicated in gain control (Atallah et al 2012;Ma et al 2010;Wilson et al 2012).…”

“…To test this hypothesis, we studied surround suppression at different levels of contrast and measured the effects of anesthesia on contrast responses; the results provide support for our hypothesis. First, we confirmed that, just as in cat and monkey, spatial integration in mouse V1 depends on stimulus contrast (see also Ayaz et al 2013;Nienborg et al 2013). At high stimulus contrast (Fig.…”

“…In primate and cat V1, spatial and temporal properties of center-surround interactions depend on stimulus contrast (Kapadia et al 1999;Sadakane et al 2006;Sceniak et al 1999;Schwabe et al 2010;Webb et al 2005). In the present study, we have shown that stimulus contrast similarly influences surround suppression in mouse V1, where lower stimulus contrast leads to larger RF center sizes and weaker suppression strength (see also Ayaz et al 2013;Nienborg et al 2013). Since anesthesia also substantially reduced contrast sensitivity, the decrease in suppression strength and the slow time course of responses under anesthesia could be attributed to anesthesia affecting contrast normalization: a full contrast stimulus presented during anesthesia might evoke comparable responses to a reduced contrast stimulus seen by an awake mouse.…”

Surround suppression and temporal processing of visual signals

“…With these results in mind, there is evidence that LGN surround suppression may contribute to the near-surround (Ishikawa et al 2010) and/or the high-contrast summation fields of V1 neurons (Angelucci and Sainsbury 2006; Ozeki et al 2004). The more extensive surrounds of cortical neurons, however, likely rely on 1) feedback from extrastriate areas, which can account for the correct spatial parameters and onset latencies of V1 suppression (Angelucci and Bressloff 2006;Bair et al 2003;Nassi et al 2013), and/or 2) somatostatin-expressing local inhibitory neurons, the optogenetic inactivation of which blocks extraclassical suppression in mouse V1 Nienborg et al 2013).…”

Control of response reliability by parvalbumin-expressing interneurons in visual cortex

“…Based on the expression of calcium-binding proteins and neuropeptides, interneurons can be classified into distinct groups 14,16,18,19 , among which parvalbumin (PV)-and somatostatin (SOM)-expressing neurons constitute a large fraction 14,19 . Recent studies have used optogenetic techniques to examine how the activities of PV and SOM interneurons influence properties such as cortical response gain, stimulus selectivity and spatial integration [20][21][22][23][24][25] . However, the effect of specific type of inhibitory interneuron on cortical response reliability remains uncharacterized.…”