Layer‐specific excitation/inhibition balances during neuronal synchronization in the visual cortex

Abstract

Rhythmic activity can synchronize neural ensembles within and across cortical layers. While gamma band rhythmicity has been observed in all layers, the laminar sources and functional impacts of neuronal synchronization in the cortex remain incompletely understood. Here, layer-specific optogenetic stimulation demonstrates that populations of excitatory neurons in any cortical layer of the mouse's primary visual cortex are sufficient to powerfully entrain neuronal oscillations in the gamma band. Within each layer, inhibition balances excitation and keeps activity in check. Across layers, translaminar output overcomes inhibition and drives downstream firing. These data establish that rhythm-generating circuits exist in all principle layers of the cortex, but provide layer-specific balances of excitation and inhibition that may dynamically shape the flow of information through cortical circuits. These data might help explain how excitation/inhibition (E/I) balances across cortical layers shape information processing, and shed light on the diverse nature and functional impacts of cortical gamma rhythms.

Wide-area all-optical neurophysiology in acute brain slices

“…Within L5 we found a heterogeneous response, where inhibition outweighed excitation in Rbp4-cre positive neurons (and possibly others which remained nonresponsive during the entire experiment) but excitation outweighed inhibition in other neurons in L5. While this paper was in review, another study interrogated the same circuit with optogenetic stimulation and simultaneous triple whole cell patch clamp, with broadly similar conclusions 35 , though the rigors of patch clamp limited the measurements to a few tens of neurons overall.…”

Transient developmental increase of prefrontal activity alters network maturation and causes cognitive dysfunction in adult mice

“…We focused on neurons from L2/3 because our previous investigations identified them as drivers of fast oscillatory rhythms at neonatal age 13 . This layer-specificity seems to be a developmental feature of mPFC, since recent work in adult sensory cortices has shown that gamma rhythms can be driven by pyramidal neurons from all layers 15,16 . We found that light-driven fast oscillatory activity increased in power and frequency across development, similarly to what we observed for spontaneous oscillations (Fig.…”

Analog closed-loop optogenetic modulation of hippocampal pyramidal cells dissociates gamma frequency and amplitude

“…A slowly increasing ramp of light (peak wavelength 590 nm) was delivered via a light-emitting diode (LED) coupled to the epifluorescence port of an upright microscope, eliciting a gamma oscillation ( Fig. 1a, b), as previously reported in rodents 10,[39][40][41][42] , cats 43 and monkeys 44 . The oscillation amplitude was reduced by approximately 60% (insets), with no net change in frequency.…”

“…A slowly increasing ramp of light (peak wavelength 590 nm) was delivered via a light-emitting diode (LED) coupled to the epifluorescence port of an upright microscope, eliciting a gamma oscillation ( Fig. 1A, B), as previously reported in rodents (Adesnik, 2018;Adesnik and Scanziani, 2010;Akam et al, 2012;Butler et al, 2016;Pastoll et al, 2013), cats (Ni et al, 2016) and monkeys (Lu et al, 2015). (C) Closed-loop oscillation clamp applied between 6 and 8 s, obtained by multiplying the ramp command by (1 + k 1 LFP + k 2 dLFP/dt), with dLFP/dt averaged over 2 ms intervals.…”