Orbitofrontal Cortex Neurons Respond to Sound and Activate Primary Auditory Cortex Neurons

Winkowski, Daniel E.; Nagode, Daniel A.; Donaldson, Kevin; Yin, Pingbo; Shamma, Shihab A.; Fritz, Jonathan B.; Kanold, Patrick O.

doi:10.1093/cercor/bhw409

Cited by 89 publications

(82 citation statements)

References 32 publications

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“…The V1-projecting OFC neurons target all three subtypes of inhibitory interneurons in V1, similar to that found for OFC projections to auditory cortex 37 and cingulate cortex projections to V1 36 . We found that optogenetic stimulation of OFC neurons in vivo preferentially activated SST interneurons in V1.…”

Section: Discussionsupporting

confidence: 76%

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Orbitofrontal control of visual cortex gain promotes visual associative learning

Liu

Deng

Zhang

et al. 2019

Preprint

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4Signaling of expected outcomes in the orbitofrontal cortex (OFC) is critical for 5 outcome-guided and learning behavior. The OFC projects to primary visual 6 cortex (V1), yet the function of this top-down projection is unclear. We found 7 that optogenetic activation of OFC projection to V1 reduced the amplitude of V1 8 visual responses via the recruitment of local somatostatin-expressing (SST) 9interneurons. Using mice performing a Go/No-Go visual task, we showed that 10 the OFC projection to V1 mediated the suppression of V1 responses to the 11 reward-irrelevant No-Go stimulus. Furthermore, the responses of V1-projecting 12 OFC neurons to No-Go stimulus were reduced when the mice's expectation was 13 incorrect. In addition, optogenetic inactivation of OFC projection to V1 14 impaired, whereas activation of SST interneurons in V1 improved the learning of 15 Go/No-Go visual task. Thus, OFC top-down projection to V1 is crucial to drive 16 visual associative learning by reducing the response gain of V1 neurons to non-17 relevant stimulus. 18 19The OFC is a critical brain region for using the information about expected 20 outcomes to guide learning and behavior 1-3 . Studies in rodents and monkeys have 21 demonstrated that the identity and expected values of specific outcomes are 22 represented by activities in the OFC 4-14 . Lesions or inactivation of the OFC impair 23 behavior guided by outcome expectancy and learning driven by the discrepancy 24 48 V1 visual response by recruiting SST interneurons. We thus hypothesized that OFC 49 projection to V1 may filter out non-relevant visual information, and tested this 50 hypothesis in mice performing a Go/No-Go visual task. We found that the OFC 51 projection to V1 contributed to the suppression of V1 responses to the No-Go 52 stimulus, which was not associated with reward. Optogenetic tagging of V1-53 projecting OFC neurons revealed that their responses to the No-Go stimulus were 54 reduced in wrong trials but not in correct trials. We further showed that optogenetic 55 inactivation of OFC projection to V1 slowed the learning of Go/No-Go visual 56 behavior. Thus, the OFC projection to V1 plays a key role in filtering out non-relevant 57 visual information to facilitate associative learning. 58 59Results 60 OFC top-down projection controls V1 response amplitude by activation of local 61SST interneurons. We injected Cholera toxin subunit B (CTB) in V1 and found that 62 the retrograde labeled neurons were in the ventrolateral OFC (vlOFC) (Fig. 1a), 63 consistent with the finding in a previous study 38 . By injecting rAAV2-retro-hSyn-Cre 64 in V1 and AAV-DIO-EYFP in the OFC, we found that the axons of OFC neurons 65 terminated in both superficial and deep layers of V1 (Fig. 1b). To examine how the 66 5 OFC top-down projection influences V1 neuronal responses, we expressed excitatory 67 opsin Channelrhodopsin-2 (ChR2) or ChrimsonR in the OFC, and measured V1 68 responses with and without laser stimulation of OFC axons in mice passively viewing 69 drifting gratings (Fig. 1c)....

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Section: Discussionsupporting

confidence: 76%

“…Frontal top-down projections to sensory cortices are known to modulate sensory processing [35][36][37] , promote accurate perception 38 , and convey predictive signals 39,40 .…”

mentioning

confidence: 99%

Orbitofrontal control of visual cortex gain promotes visual associative learning

Liu

Deng

Zhang

et al. 2019

Preprint

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“…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). Thus, the difference between engaged and disengaged sensitivity is a proxy for the strength of a top-down mechanism.…”

Section: Significancementioning

confidence: 99%

“…For our purposes, top-down refers to the functional influence of a higher-order brain region on neural activity in ACx, brought about by task engagement. Several plausible candidate regions may mediate this top-down effect, either in isolation or in concert with one another, including frontal cortex (50,51), nucleus basalis (73)(74)(75), locus coeruleus (76), ventral tegmental area (77,78), and multisensory cortex (17).…”

Section: Significancementioning

confidence: 99%

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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“…We know of no existing evidence that the prefrontal cortex influences responses in the IC. However, neurons in the orbitofrontal regions respond to sound and via descending connections influence sound processing in auditory cortex (Saunders et al, 1985;Fritz et al, 2010;Schneider et al, 2014;Winkowski et al, 2018). These prefrontal cortical regions have a central role in executive function and exert task-dependent influences on sensory processing (Öngür and Price, 2000).…”

Section: Auditory and Non-auditory Cortico-collicular Projectionsmentioning

confidence: 99%

Multiple non-auditory cortical regions innervate the auditory midbrain

Olthof

Rees

Gartside

2019

Preprint

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Our perceptual experience of sound depends on the integration of multiple sensory and cognitive domains, but the networks sub-serving this integration are unclear. There are connections linking different cortical domains, however we do not know if there are also connections between multiple cortical domains and subcortical structures. Retrograde tracing in rats revealed that the inferior colliculus -the auditory midbrain -receives dense descending projections from not only the auditory cortex, but also the visual, somatosensory, motor, and prefrontal cortices. While all these descending connections are bilateral, those from sensory areas show a more pronounced ipsilateral dominance than those from motor and prefrontal cortices. Anterograde tracing from cortical areas identified by retrograde tracing, showed cortical fibres terminating in all three subdivisions of the inferior colliculus, targeting both inhibitory and excitatory neurons. These findings demonstrate that auditory perception is served by a network that includes extensive descending connections from sensory, behavioural, and executive cortices.

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Orbitofrontal Cortex Neurons Respond to Sound and Activate Primary Auditory Cortex Neurons

Cited by 89 publications

References 32 publications

Orbitofrontal control of visual cortex gain promotes visual associative learning

Orbitofrontal control of visual cortex gain promotes visual associative learning

Top-down modulation of sensory cortex gates perceptual learning

Multiple non-auditory cortical regions innervate the auditory midbrain

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