Cortico-cortical feedback from V2 exerts a powerful influence over the visually evoked local field potential and associated spike timing in V1

Abstract

The local field potential (LFP) is generally thought to be dominated by synaptic activity within a few hundred microns of the recording electrode. The sudden onset of a visual stimulus causes a large downward deflection of the LFP recorded in primary visual cortex, known as a visually evoked potential (VEP), followed by rhythmic oscillations in the gamma range (30-80 Hz) that are often in phase with action potentials of nearby neurons. By inactivating higher visual areas that send feedback projections to V1, we produced a large decrease in amplitude of the VEP, and a strong attenuation of gamma rhythms in both the LFP and multi-unit activity, despite an overall increase in neuronal spike rates. Our results argue that much of the recurrent, rhythmic activity measured in V1 is strongly gated by feedback from higher areas, consistent with models of coincidence detection that result in burst firing by layer 5 pyramidal neurons.

Illusions, Delusions, and Your Backwards Bayesian Brain: A Biased Visual Perspective

“…4b, c; Adesnik et al, 2012]. Further strengthening the possible association between cortico-cortical feedback and SST neurons, we discovered a dramatic reduction in visually evoked gamma oscillations in macaque V1 when inactivating V2/V3 [Hartmann et al, 2019], similar to that observed in mouse V1 with local SST inactivation [Fig. 4d, e;Veit et al, 2017].…”

“…Second, we observed that the delayed component (∼100-200 ms after stimulus onset) of the visually evoked potential (VEP) in V1 was greatly reduced in amplitude during V2/V3 cooling [Hartmann et al, 2019]. We think that a switch from burst mode to single-spiking [Larkum et al, 1999], whether mediated by SST neurons or by a direct effect of feedback on the apical dendrites of layer 5 PCs, could account for the reduced spiking variability [Gómez-Laberge et al, 2016] and might, at least partially, explain feedback's powerful influence over the volley of recurrent activity that follows the initial feedforward response in the VEP [Hartmann et al, 2019].…”

Uncovering circuit mechanisms of current sinks and sources with biophysical simulations of primary visual cortex

“…Hartmann et al (2019) found that feedback from higher visual areas (HVAs) can exert a powerful influence on the magnitude of the evoked LFP response recorded in V1 of macaque monkeys, particularly in the period 80-100 ms after stimulus onset. The sustained L2/3 sink and L4 source we observe in the experimental CSD emerge at 60 ms (Fig.…”

“…3C). Furthermore, anatomical data indicate that synapses from HVAs terminate on L1 and L2/3 apical dendrites of pyramidal cells (whose cell bodies reside in L2/3 or L5) (Glickfeld and Olsen, 2017; Marques et al, 2018; Hartmann et al, 2019; Keller et al, 2020; Shen et al, 2020). Together, these observations suggest that the sustained L2/3 sink and L4 source might, in part, be induced by feedback from higher visual areas (HVA), where the sink is generated from the input to the apical tufts in L1 and L2/3, and the source may be the return currents of this input.…”

“…This suggests that utilizing the CSD in the optimization of the model can provide constraints on the circuit architecture that could not be obtained from spikes alone. Hartmann et al (2019) found that feedback from higher visual areas (HVAs) can exert a powerful influence on the magnitude of the evoked LFP response recorded in V1 of macaque monkeys, particularly in the period 80-100 ms after stimulus onset. The sustained L2/3 sink and L4 source we observe in the experimental CSD emerge at 60 ms (Fig.…”