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:10.1088/1741-2552/ab39cf

Cited by 25 publications

(17 citation statements)

References 55 publications

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“…Besides, one would also anticipate that prediction neurons would have their strongest impact when peripheral signals are weak (i.e., the Kalman gain would be highest under these circumstances). Consistent with this idea, previous work has shown that top-down modulation tends to be strongest in broadly tuned neurons [presumably neurons with ambiguous frequency representations (Vila et al, 2019) or when acoustic stimulus amplitude is weak (Jen et al, 1998)]. It may be the case that neurons that are broadly tuned to isolated sounds may be more sharply tuned in other contexts.…”

Section: Conclusion and Future Challengesmentioning

confidence: 69%

“…Importantly, the specific protocol of electrical stimulation may make a large difference in the impact on subcortical neurons. Small changes in the relative timing of cortical vs. acoustic stimulation, relative amplitudes, pulse rates, etc, can change responses from excitatory to inhibitory, even with optogenetic stimulation (Guo et al, 2017;Vila et al, 2019). Also, many studies have used stimulation paradigms that are really perceptual learning paradigms.…”

Section: Methodological Issues In Top-down Modulation In the Subcortical Auditory Systemmentioning

confidence: 99%

See 1 more Smart Citation

Top-Down Inference in the Auditory System: Potential Roles for Corticofugal Projections

Asilador

Llano

2021

Front. Neural Circuits

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It has become widely accepted that humans use contextual information to infer the meaning of ambiguous acoustic signals. In speech, for example, high-level semantic, syntactic, or lexical information shape our understanding of a phoneme buried in noise. Most current theories to explain this phenomenon rely on hierarchical predictive coding models involving a set of Bayesian priors emanating from high-level brain regions (e.g., prefrontal cortex) that are used to influence processing at lower-levels of the cortical sensory hierarchy (e.g., auditory cortex). As such, virtually all proposed models to explain top-down facilitation are focused on intracortical connections, and consequently, subcortical nuclei have scarcely been discussed in this context. However, subcortical auditory nuclei receive massive, heterogeneous, and cascading descending projections at every level of the sensory hierarchy, and activation of these systems has been shown to improve speech recognition. It is not yet clear whether or how top-down modulation to resolve ambiguous sounds calls upon these corticofugal projections. Here, we review the literature on top-down modulation in the auditory system, primarily focused on humans and cortical imaging/recording methods, and attempt to relate these findings to a growing animal literature, which has primarily been focused on corticofugal projections. We argue that corticofugal pathways contain the requisite circuitry to implement predictive coding mechanisms to facilitate perception of complex sounds and that top-down modulation at early (i.e., subcortical) stages of processing complement modulation at later (i.e., cortical) stages of processing. Finally, we suggest experimental approaches for future studies on this topic.

show abstract

Section: Conclusion and Future Challengesmentioning

confidence: 69%

Section: Methodological Issues In Top-down Modulation In the Subcortical Auditory Systemmentioning

confidence: 99%

Top-Down Inference in the Auditory System: Potential Roles for Corticofugal Projections

Asilador

Llano

2021

Front. Neural Circuits

View full text Add to dashboard Cite

show abstract

“…Importantly, the specific protocol of electrical stimulation may make a large difference on the impact on subcortical neurons. Small changes in the relative timing of cortical vs. acoustic stimulation, relative amplitudes, pulse rates, etc, can change responses from excitatory or inhibitory, even with optogenetic stimulation (Guo et al, 2017;Vila et al, 2019). In addition, many studies have used stimulation paradigms that are really perceptual learning paradigms.…”

Section: Early Vs Late Top-down Modulationmentioning

confidence: 99%

“…In addition, one would also anticipate that prediction neurons would have their strongest impact when peripheral signals are weak (i.e., the Kalman gain would be highest under these circumstances). Consistent with this idea., previous work has shown that top-down modulation tends to be strongest in broadly tuned neurons (presumably neurons with ambiguous frequency representations (Vila et al, 2019) or when acoustic stimulus amplitude is weak (Jen et al, 1998b)). It may be the case that neurons that are broadly tuned to isolated sounds may be more sharply tuned in other contexts.…”

Section: Conclusion and Future Challengesmentioning

confidence: 99%

Top-down inference in the auditory system: Potential roles for corticofugal projections

Asilador¹,

Llano²

2020

Preprint

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It has become widely accepted that humans use contextual information to infer the meaning of ambiguous acoustic signals. In speech, for example, high-level semantic, syntactic or lexical information shape our understanding of a phoneme buried in noise. Most current theories to explain this phenomenon rely on hierarchical predictive coding models involving a set of Bayesian priors emanating from high-level brain regions (e.g., prefrontal cortex) that are used to influence processing at lower-levels of the sensory hierarchy (e.g., auditory cortex). As such, virtually all proposed models to explain top-down facilitation are focused on the cerebral cortex, and consequently subcortical nuclei have scarcely been discussed in this context. However, subcortical auditory nuclei receive massive, heterogeneous and cascading descending projections at every level of the sensory hierarchy, and activation of these systems has been shown to improve speech recognition. It is not yet clear whether or how top-down modulation to resolve ambiguous sounds calls upon these corticofugal projections. Here, we review the literature on top-down modulation in the auditory system, primarily focused on humans and cortical imaging/recording methods, and attempt to relate these findings to a growing animal literature, which has primarily been focused on corticofugal projections. We argue that corticofugal pathways contain the requisite circuitry to implement predictive coding mechanisms to facilitate perception of complex sounds and that top-down modulation at early stages of processing complements modulation at later (i.e., cortical) stages of processing. Finally, we suggest experimental approaches for future studies on this topic.

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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; Yan and Suga, 1998, 1999; Nwabueze-Ogbo et al, 2002; Xiao and Suga, 2002; Yu et al, 2004; Nakamoto et al, 2008, 2010; Anderson 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 25 publications

References 55 publications

Top-Down Inference in the Auditory System: Potential Roles for Corticofugal Projections

Top-Down Inference in the Auditory System: Potential Roles for Corticofugal Projections

Top-down inference in the auditory system: Potential roles for corticofugal projections

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

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