Optimizing optogenetic stimulation protocols in auditory corticofugal neurons based on closed-loop spike feedback

Vila, Charles-Henri; Williamson, R. S.; Hancock, Kenneth E.; Polley, Daniel B.

doi:10.1101/505214

Cited by 3 publications

(4 citation statements)

References 47 publications

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“…In our study we were able to record from a larger neuronal population, revealing a subset of neurons in central IC that were modulated by feedback. This is consistent with another study which observed enhanced white noiseinduced activity in a small subset of neurons in the central nucleus of IC with activation of direct cortico-collicular feedback (Vila et al, 2019). The effects in central IC may be due to direct cortico-collicular feedback, intracollicular circuits (Saldaña and Merchań, 1992;Malmierca et al, 1995;Miller et al, 2005;Sturm et al, 2014) , or a combination of these mechanisms.…”

Section: Discussionsupporting

confidence: 92%

“…Stimulation of AC had mixed effects on sound-evoked responses in IC, increasing and decreasing responses in different subpopulations of neurons (Jen et al, 1998;Zhou and Jen, 2005). Consistent with this effect, different patterns of direct corticocollicular activation enhanced or suppressed white noise-induced responses in IC (Vila et al, 2019). AC inactivation studies, on the other hand, found less consistent effects on IC responses.…”

Section: Introductionmentioning

confidence: 70%

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Auditory cortex shapes sound responses in the inferior colliculus

Blackwell

Lesicko

Rao

et al. 2019

Preprint

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The extensive feedback from the auditory cortex (AC) to the inferior colliculus (IC) supports critical aspects of auditory learning, but has not been extensively characterized. Furthermore, it remains unknown whether and how intra-cortical processing of auditory information propagates to earlier stages in the auditory pathway. Previous studies demonstrated that responses of neurons in IC are altered by focal electrical stimulation and pharmacological inactivation of auditory cortex, but these methods lack the ability to selectively manipulate the activity of projection neurons. Combining viral technology with electrophysiological recordings, we measured the effects of selective optogenetic activation or suppression of cortico-collicular feedback projections on IC responses to sounds. Activation of cortico-collicular feedback generally increased spontaneous activity and decreased stimulus selectivity in IC, whereas suppression of the feedback did not affect collicular activity. To further understand how microcircuits in the auditory cortex may control collicular activity, we tested the effects of optogenetically modulating different cortical neuronal subtypes, specifically parvalbumin-positive (PV) and somatostatin-positive (SOM) inhibitory interneurons. We found that, despite strong effects on sound-evoked responses across the layers of AC, activating either type of interneuron did not affect IC sound-evoked activity. However, suppression of SOMs, but not PVs, weakly increased spontaneous activity in IC. These findings suggest that shaping of sound responses mediated by cortical inhibition does not affect sound processing in IC. Combined, our results identify that activation of excitatory projections, but not inhibitory-driven increases in cortical activity, affects collicular sound responses. Significance StatementDescending projections from the auditory cortex to the auditory midbrain, the inferior colliculus, have been shown to play a critical role in auditory learning and behavior. However, little is known about the details of how this direct feedback shapes neuronal responses to sounds in the inferior colliculus. We found that direct activation of cortico-collicular feedback increased spontaneous and modulated sound-evoked activity in the inferior colliculus. Interestingly, modulation of inhibitory interneuron activity, thereby increasing or decreasing excitatory neuronal activity in the auditory cortex, did not affect sound responses in the inferior colliculus. This work offers evidence that auditory cortex shapes sound responses in the inferior colliculus via direct feedback independently of the activity of cortical inhibitory interneurons.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 70%

Auditory cortex shapes sound responses in the inferior colliculus

Blackwell

Lesicko

Rao

et al. 2019

Preprint

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“…The temporal profile of vS1 sensory responses was conserved under optogenetic excitation 21 . Figure 3c, left, shows the population peristimulus time histogram (PSTH) in EYFP-ChR2(H134R)-expressing rats in the absence of optogenetic excitation.…”

Section: Time Codingmentioning

confidence: 97%

The sensory code within sense of time

Reinartz

Fassihi

Paz

et al. 2021

Preprint

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Sensory experiences are accompanied by the perception of the passage of time; a cell phone vibration, for instance, is sensed as brief or long. The neuronal mechanisms underlying the perception of elapsed time remain unknown1. Recent work agrees on a role for cortical processing networks2,3, however the causal function of sensory cortex in time perception has not yet been specified. We hypothesize that the mechanisms for time perception are embedded within primary sensory cortex and are thus governed by the basic rules of sensory coding. By recording and optogenetically modulating neuronal activity in rat vibrissal somatosensory cortex, we find that the percept of stimulus duration is dilated and compressed by optogenetic excitation and inhibition, respectively, during stimulus delivery. A second set of rats judged the intensity of tactile stimuli; here, optogenetic excitation amplified the intensity percept, demonstrating sensory cortex to be the common gateway to both time and stimulus feature processing. The coding algorithms for sensory features are well established4–10. Guided by these algorithms, we formulated a 3–stage model beginning with the membrane currents evoked by vibrissal and optogenetic drive and culminating in the representation of perceived time; this model successfully replicated rats′ choices. Our finding that stimulus coding is intrinsic to sense of time disagrees with dedicated pacemaker-accumulator operation models11–13, where sensory input acts only to trigger the onset and offset of the timekeeping process. Time perception is thus as deeply intermeshed within the sensory processing pathway as is the sense of touch itself14,15 and can now be treated through the computational language of sensory coding. The model presented here readily generalizes to humans14,16 and opens up new approaches to understanding the time misperception at the core of numerous neurological conditions17,18.

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“…These corticofugal projections likely play a major role in hearing by providing an anatomical substrate for "top-down" information to control early acoustic processing. Indeed, stimulating or silencing the auditory cortex in vivo changes spontaneous and sound-evoked activity throughout the central auditory system (Massopust and Ordy, 1962;Ryugo and Weinberger, 1976;Suga, 1998, 1999;Xiao and Suga, 2002;Yu et al, 2004;Nakamoto et al, 2008Nakamoto et al, , 2010Anderson and Malmierca, 2013;Kong et al, 2014;Vila et al, 2019;Blackwell et al, 2020;Qi et al, 2020), indicating that high-level activity regulates the moment-to-moment function of sub-cortical auditory circuits. However, little is known regarding the biophysical properties of auditory corticofugal synapses, nor do we understand how descending signals are integrated with ascending information.…”

Section: Introductionmentioning

confidence: 99%

Synaptic Mechanisms of Top-Down Control in the Non-Lemniscal Inferior Colliculus

Oberle

Ford

Dileepkumar

et al. 2021

Preprint

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Corticofugal projections to evolutionarily ancient, sub-cortical structures are ubiquitous across mammalian sensory systems. These descending pathways enable the neocortex to control ascending sensory representations in a predictive or feedback manner, but the underlying cellular mechanisms are poorly understood. Here we combine optogenetic approaches with in vivo and in vitro patch-clamp electrophysiology to study the projection from auditory cortex to the inferior colliculus (IC), a major descending auditory pathway that controls IC neuron feature selectivity, plasticity and auditory perceptual learning. Although individual auditory cortico-collicular synapses were generally weak, IC neurons often integrated inputs from multiple corticofugal axons that generated reliable, tonic depolarizations even during prolonged presynaptic activity. Latency measurements in vivo showed that descending signals reach the IC within 30 ms of sound onset, which in IC neurons corresponded to the peak of synaptic depolarizations evoked by short sounds. Activating ascending and descending pathways at latencies expected in vivo caused a NMDA receptor dependent, supra-linear EPSP summation, indicating that descending signals can non-linearly amplify moment-to-moment acoustic responses. Our results shed light upon the synaptic bases of descending sensory control, and imply that heterosynaptic cooperativity contributes to sub-cortical plasticity and perceptual learning.

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Optimizing optogenetic stimulation protocols in auditory corticofugal neurons based on closed-loop spike feedback

Cited by 3 publications

References 47 publications

Auditory cortex shapes sound responses in the inferior colliculus

Auditory cortex shapes sound responses in the inferior colliculus

The sensory code within sense of time

Synaptic Mechanisms of Top-Down Control in the Non-Lemniscal Inferior Colliculus

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