A Decline in Response Variability Improves Neural Signal Detection during Auditory Task Performance

Trapp, Gardiner von; Buran, Bradley N.; Sen, Kamal; Semple, Malcolm N.; Sanes, Dan H.

doi:10.1523/jneurosci.1302-16.2016

Cited by 59 publications

(63 citation statements)

References 66 publications

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“…This result is in line with an abundance of work demonstrating behaviorally gated modulations of ACx activity (37,(44)(45)(46)(47)(48)(49)(62)(63)(64)(65)(66). Our observation that disengaged neural sensitivity is better if measured immediately after behavioral testing, rather than before (compare green lines in Fig.…”

Section: Significancesupporting

confidence: 88%

“…Extracellular single-and multiunit activity was recorded from left ACx as described previously (37,90). Firing rates were transformed to d′ values and fit with logistic functions (37).…”

Section: Methodsmentioning

confidence: 99%

“…Improvements in neural sensitivity could be due to an increased separation of warn-and safe-evoked FR distributions (13), and/or a reduction in FR variability across training days (20)(21)(22)(23)37). As illustrated for one representative multiunit in Fig.…”

Section: Significancementioning

confidence: 99%

“…Here, we adopt the term "top-down" to mean the functional influence of a descending projection from one or more brain regions on neural activity in sensory cortex. A commonly used procedure to assess the magnitude of top-down mechanisms is to compare neural responsiveness during two different states of behavioral engagement (37,(44)(45)(46)(47)(48)(49). Specifically, top-down inputs are thought to actively modulate ACx responses during task performance (or "engagement") but not during nontask ("disengaged") listening sessions (50,51).…”

Section: Significancementioning

confidence: 99%

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Top-down modulation of sensory cortex gates perceptual learning

Caras

Sanes

2017

Proc. Natl. Acad. Sci. U.S.A.

104

108

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Practice sharpens our perceptual judgments, a process known as perceptual learning. Although several brain regions and neural mechanisms have been proposed to support perceptual learning, formal tests of causality are lacking. Furthermore, the temporal relationship between neural and behavioral plasticity remains uncertain. To address these issues, we recorded the activity of auditory cortical neurons as gerbils trained on a sound detection task. Training led to improvements in cortical and behavioral sensitivity that were closely matched in terms of magnitude and time course. Surprisingly, the degree of neural improvement was behaviorally gated. During task performance, cortical improvements were large and predicted behavioral outcomes. In contrast, during nontask listening sessions, cortical improvements were weak and uncorrelated with perceptual performance. Targeted reduction of auditory cortical activity during training diminished perceptual learning while leaving psychometric performance largely unaffected. Collectively, our findings suggest that training facilitates perceptual learning by strengthening both bottom-up sensory encoding and top-down modulation of auditory cortex.broad range of sensory skills improve with practice during perceptual learning (PL), including language acquisition (1-3), musical abilities (4), and recognition of emotions (5). The neural bases for such perceptual improvement may vary widely. For example, training-based changes in neural activity have been identified in a number of brain regions, including early (6-13) and late (14, 15) sensory cortices, multisensory regions (16, 17), and downstream decision-making areas (18). Similarly, several neural mechanisms have been proposed, such as enhanced signal representation (19), reduction of external (20, 21) or internal (22, 23) noise, and improvement in sensory readout or decision making (13,18,24,25).The apparent divergence of loci and mechanisms associated with PL could be due, in part, to limitations of experimental design. For example, some neural changes associated with PL are transient (26-29), making it necessary to monitor neural activity throughout the duration of perceptual training, rather than making comparisons only after PL is complete (6-12, 14-16, 30). For similar reasons, it is critical to block the function of a specific candidate brain region during training to determine whether it plays a causal role in PL. Although some reports show that manipulating brain activity can influence PL (28,(31)(32)(33)(34), there are no loss-of-function experiments to determine whether a particular region is required for behavioral improvement.To address these unresolved issues, we recorded from auditory cortex (ACx) as animals improved on an auditory detection task and, in separate experiments, blocked ACx activity during the period of perceptual training. We found that neural and behavioral sensitivity improved in a nearly identical manner over the course of training, in terms of both absolute magnitude and kinetics. Furthermore,...

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Section: Significancesupporting

confidence: 88%

“…Extracellular single-and multiunit activity was recorded from left ACx as described previously (37,90). Firing rates were transformed to d′ values and fit with logistic functions (37).…”

Section: Methodsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

See 2 more Smart Citations

Top-down modulation of sensory cortex gates perceptual learning

Caras

Sanes

2017

Proc. Natl. Acad. Sci. U.S.A.

104

108

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show abstract

“…active conditions and between attend-toward vs. attend-away conditions (Niwa et al, 2012b;Schwartz and David, 2017;von Trapp et al, 2016).…”

Section: Average A1 Neurons' Feature Sensitivity Is Constant Across Amentioning

confidence: 99%

An emergent population code in primary auditory cortex supports selective attention to spectral and temporal sound features

Downer¹,

Verhein

Rapone³

et al. 2020

Preprint

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Textbook descriptions of primary sensory cortex (PSC) revolve around single neurons' representation of low-dimensional sensory features, such as visual object orientation in V1, location of somatic touch in S1, and sound frequency in A1. Typically, studies of PSC measure neurons' responses along few (1 or 2) stimulus and/or behavioral dimensions. However, real-world stimuli usually vary along many feature dimensions and behavioral demands change constantly. In order to illuminate how A1 supports flexible perception in rich acoustic environments, we recorded from A1 neurons while rhesus macaques performed a feature-selective attention task. We presented sounds that varied along spectral and temporal feature dimensions (carrier bandwidth and temporal envelope, respectively). Within a block, subjects attended to one feature of the sound in a selective change detection task. We find that single neurons tend to be highdimensional, in that they exhibit substantial mixed selectivity for both sound features, as well as task context. Contrary to common findings in many previous experiments, attention does not enhance the single-neuron representation of attended features in our data. However, a population-level analysis reveals that ensembles of neurons exhibit enhanced encoding of attended sound features, and this population code tracks subjects' performance. Importantly, surrogate neural populations with intact singleneuron tuning but shuffled higher-order correlations among neurons failed to yield attention-related effects observed in the intact data. These results suggest that an emergent population code not measurable at the single-neuron level might constitute the functional unit of sensory representation in PSC. SIGNIFICANCE STATEMENTThe ability to adapt to a dynamic sensory environment promotes a range of important natural behaviors. We recorded from single neurons in monkey primary auditory cortex while subjects attended to either the spectral or temporal features of complex sounds.Surprisingly, we find no average increase in responsiveness to, or encoding of, the attended feature across single neurons. However, when we pool the activity of the sampled neurons via targeted dimensionality reduction, we find enhanced populationlevel representation of the attended feature and suppression of the distractor feature.This dissociation of the effects of attention at the level of single neurons vs. the population highlights the synergistic nature of cortical sound encoding and enriches our understanding of sensory cortical function.

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Organization of orbitofrontal‐auditory pathways in the Mongolian gerbil

Ying

Hamlette

Nikoobakht

et al. 2023

J of Comparative Neurology

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Sound perception is highly malleable, rapidly adjusting to the acoustic environment and behavioral demands. This flexibility is the result of ongoing changes in auditory cortical activity driven by fluctuations in attention, arousal, or prior expectations. Recent work suggests that the orbitofrontal cortex (OFC) may mediate some of these rapid changes, but the anatomical connections between the OFC and the auditory system are not well characterized. Here, we used virally mediated fluorescent tracers to map the projection from OFC to the auditory midbrain, thalamus, and cortex in a classic animal model for auditory research, the Mongolian gerbil (Meriones unguiculatus). We observed no connectivity between the OFC and the auditory midbrain, and an extremely sparse connection between the dorsolateral OFC and higher order auditory thalamic regions. In contrast, we observed a robust connection between the ventral and medial subdivisions of the OFC and the auditory cortex, with a clear bias for secondary auditory cortical regions. OFC axon terminals were found in all auditory cortical lamina but were significantly more concentrated in the infragranular layers. Tissue‐clearing and lightsheet microscopy further revealed that auditory cortical‐projecting OFC neurons send extensive axon collaterals throughout the brain, targeting both sensory and non‐sensory regions involved in learning, decision‐making, and memory. These findings provide a more detailed map of orbitofrontal‐auditory connections and shed light on the possible role of the OFC in supporting auditory cognition.

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A Decline in Response Variability Improves Neural Signal Detection during Auditory Task Performance

Cited by 59 publications

References 66 publications

Top-down modulation of sensory cortex gates perceptual learning

Top-down modulation of sensory cortex gates perceptual learning

An emergent population code in primary auditory cortex supports selective attention to spectral and temporal sound features

Organization of orbitofrontal‐auditory pathways in the Mongolian gerbil

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