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

Abstract

The responses of visual cortical neurons to natural stimuli are both reliable and sparse. These properties require inhibition, yet the contribution of specific types of inhibitory neurons is not well understood. Here we demonstrate that optogenetic suppression of parvalbumin (PV)-but not somatostatin (SOM)-expressing interneurons reduces response reliability in the primary visual cortex of anaesthetized and awake mice. PV suppression leads to increases in the low firing rates and decreases in the high firing rates of cortical neurons, resulting in an overall reduction of the signal-to-noise ratio (SNR). In contrast, SOM suppression generally increases the overall firing rate for most neurons, without affecting the SNR. Further analysis reveals that PV, but not SOM, suppression impairs neural discrimination of natural stimuli. Together, these results reveal a critical role for PV interneurons in the formation of reliable visual cortical representations of natural stimuli.

Basal forebrain activation enhances between-trial reliability of low-frequency local field potentials (LFP) and spiking activity in tree shrew primary visual cortex (V1)

“…It is thus likely that GABAergic BF projections contribute to the effects reported here. In addition, it is probable that GABAergic cortical interneurons also contribute to reliability regulation, based on recent results showing that suppression of parvalbumin GABAergic interneuron activity in rodent V1 decreases response reliability (Zhu et al 2015), and pharmacological GABA blockade in macaque extrastriate visual cortex enhances Fano factors (Thiele et al 2012). Our findings thus argue for an involvement of both cortical and BF GABAergic cells, as well as an important cholinergic contribution to reliability effects, which is most likely mediated by M2 muscarinic ACh receptors.…”

Somatostatin Interneurons Control a Key Component of Mismatch Negativity in Mouse Visual Cortex

“…SOMs are a strong candidate for MMN processing given their: i) late input/output facilitation (or amplification) in the MMN time-range (Karnani et al, 2014), ii) a capacity for both inhibition and dis-inhibition of neighboring pyramidal neurons (Cottam et al, 2013), and iii) preferential inhibition of the local neuronal network to redundant stimuli compared to deviants (Natan et al, 2015). These characteristics lie in contrast to other more commonly studied interneuron types, such as parvalbumin containing cells (Cottam et al, 2013; Karnani et al, 2014; Natan et al, 2015; Zhu et al, 2015). …”

“…These results held true for non-normalized values (Fig S4g,h). SOM suppression, importantly, did not alter evoked calcium transients to control stimuli in responsive neurons (first 500ms, F (1,64) SOM-hM4D =1.66, p=.20; Fig S4d-h), but did produce a trend-level increase in responses to non-preferred stimulus orientations ( F (1,89) SOM-hM4D =3.24, p=.07 ; repeated measures ANOVA on magnitudes 90 deg from peak response; Fig S4d), Previous work has reported either small increases (Zhu et al, 2015) or no change in neuronal responses to visual stimuli after SOM-suppression (Chen et al, 2015b), consistent with their concurrent roles in subtractive inhibition and pyramidal cell disinhibition in V1 (Cottam et al, 2013). …”

Inhibitory control of correlated intrinsic variability in cortical networks

“…While the exact roles played by different inhibitory neuron types are still under investigation (Lee et al, 2014; Seybold et al, 2015), the activation of inhibitory interneurons generally results in sharper tuning, weaker correlations, and enhanced behavioral performance (Wilson et al, 2012; Lee et al, 2012; Chen et al, 2015), while suppression of inhibitory interneurons has the opposite effect, decreasing the signal-to-noise ratio and reliability of evoked responses across trials (Zhu et al, 2015; Chen et al, 2015). These results demonstrate that increased inhibition enhances sensory processing and are consistent with the overall suppression of cortical activity that is often observed during active behaviors (Otazu et al, 2009; Schneider et al, 2014; Kuchibhotla et al, 2016; Buran et al, 2014).…”