Auditory cortex ensembles jointly encode sound and locomotion speed to support sound perception during movement

PLoS Biology, Journal Year: 2023, Volume and Issue: 21(8), P. e3002277 - e3002277

Published: Aug. 31, 2023

The ability to process and act upon incoming sounds during locomotion is critical for survival adaptive behavior. Despite the established role that auditory cortex (AC) plays in behavior- context-dependent sound processing, previous studies have found cortical activity on average suppressed as compared immobility. While suppression of responses self-generated results from corollary discharge, which weakens predictable sounds, functional weaker unpredictable external remains unclear. In particular, whether sound-evoked reflects reduced involvement AC processing or it masking by an alternative neural computation this state unresolved. Here, we tested hypothesis rather than simple inhibition, reflect a tradeoff with emergence explicit reliable coding velocity. To test hypothesis, first used inactivation behaving mice sound-guided behavior locomotion. investigate nature two-photon calcium imaging local excitatory populations awake mice. We had diverse influences different neurons, net baseline-subtracted stimulus detection, consistent studies. Importantly, inhibitory effect was strongly shaped elevated ongoing compressed response dynamic range, reflecting enhanced “noise,” reliably encoded animal’s speed. Decoding analyses revealed speed are robustly co-encoded ensemble activity. Finally, patterns joint electrophysiologically recorded freely moving rats. Together, our data suggest being locomotion, ensembles explicitly encode alongside information support perception

Language: Английский

---

Action does not enhance but attenuates predicted touch

eLife, Journal Year: 2023, Volume and Issue: 12

Published: Dec. 15, 2023

Dominant motor control theories propose that the brain predicts and attenuates somatosensory consequences of actions, referred to as attenuation. Support comes from psychophysical neuroimaging studies showing touch applied on a passive hand elicits attenuated perceptual neural responses if it is actively generated by one's other hand, compared an identical external origin. However, recent experimental findings have challenged this view providing evidence perceived intensity enhanced active does not receive simultaneously with (somatosensory enhancement) further attributing attenuation double tactile stimulation hands upon contact. Here, we directly contrasted hypotheses enhancement models regarding how action influences perception manipulating whether contacts hand. We assessed in absence any predictive cues condition turned out be essential for interpreting findings. In three pre-registered experiments, demonstrate enhance predicted (Experiment 1), previously reported 'enhancement' effects are driven reference used 2), self-generated robustly regardless two make contact 3). Our results provide conclusive but prompt reappraisal which theoretical frameworks proposing prediction based.

Language: Английский

---

Expectation violations produce error signals in mouse V1

Cerebral Cortex, Journal Year: 2023, Volume and Issue: 33(13), P. 8803 - 8820

Published: May 13, 2023

Abstract Repeated exposure to visual sequences changes the form of evoked activity in primary cortex (V1). Predictive coding theory provides a potential explanation for this, namely that plasticity shapes cortical circuits encode spatiotemporal predictions and subsequent responses are modulated by degree which actual inputs match these expectations. Here we use recently developed statistical modeling technique called Model-Based Targeted Dimensionality Reduction (MbTDR) study visually dynamics mouse V1 context an experimental paradigm “sequence learning.” We report spiking changed significantly with training, manner generally consistent predictive framework. Neural expected stimuli were suppressed late window (100–150 ms) after stimulus onset following whereas novel not. Substituting familiar one led increases firing persisted at least 300 ms. Omitting predictable trained animals also increased time onset. Finally, show data can be used accurately decode within sequence. Our findings idea early is involved information.

Language: Английский

---

Movement-related modulation in mouse auditory cortex is widespread yet locally diverse

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: July 3, 2023

ABSTRACT Neurons in the mouse auditory cortex are strongly influenced by behavior, including both suppression and enhancement of sound-evoked responses during movement. The comprises multiple fields with different roles sound processing distinct connectivity to movement-related centers brain. Here, we asked whether modulation might differ across cortical fields, thereby contributing heterogeneity at single-cell level. We used wide-field calcium imaging identify followed cellular-resolution two-photon visualize activity layer 2/3 excitatory neurons within each field. measured neuron’s three categories (pure tones, chirps, amplitude modulated white noise) as mice rested ran on a non-motorized treadmill. found that individual field typically respond just one category. Some only active rest others locomotion, those responsive conditions retain their sound-category tuning. effects locomotion vary single cell level, neural responses, net modulatory effect is largely conserved fields. Movement-related also reflects more complex behavioral patterns, instantaneous running speed non-locomotor movements such grooming postural adjustments, similar patterns seen all Our findings underscore complexity throughout indicate movement related widespread phenomenon. SIGNIFICANCE STATEMENT Throughout sensory cortex, behavior. It remains unknown primary higher-order similarly or differentially show locally heterogeneous, but macroscopic conserved. These data highlight nature suggest signals may inform computations nodes cortex.

Language: Английский

---

Cooperative thalamocortical circuit mechanism for sensory prediction errors

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: July 12, 2023

Abstract The brain functions as a prediction machine, utilizing an internal model of the world to anticipate sensations and outcomes our actions. Discrepancies between expected actual events, referred errors, are leveraged update guide attention towards unexpected events 1–10 . Despite importance error signals for various neural computations across multiple regions, surprisingly little is known about circuit mechanisms responsible their implementation. Here we describe thalamocortical disinhibitory required generating sensory errors in mouse primary visual cortex (V1). Using calcium imaging with optogenetic manipulations mice traverse familiar virtual environment, show that violation animals’ predictions by stimulus preferentially boosts responses layer 2/3 V1 neurons most selective stimulus. Prediction specifically amplify input, rather than representing non-specific surprise or difference signal how input deviates from predictions. Selective amplification implemented cooperative mechanism requiring thalamic pulvinar, cortical vasoactive-intestinal-peptide-expressing (VIP) inhibitory interneurons. In response VIP inhibit specific subpopulation somatostatin-expressing (SOM) interneurons gate excitatory pulvinar V1, resulting pulvinar-driven response-amplification stimulus-selective V1. Therefore, prioritizes unpredicted information selectively increasing salience features through synergistic interaction neocortical circuits.

Language: Английский

---

Dynamic changes in somatosensory and cerebellar activity mediate temporal recalibration of self-touch

Communications Biology, Journal Year: 2024, Volume and Issue: 7(1)

Published: May 3, 2024

Abstract An organism’s ability to accurately anticipate the sensations caused by its own actions is crucial for a wide range of behavioral, perceptual, and cognitive functions. Notably, sensorimotor expectations produced when touching one’s body attenuate such sensations, making them feel weaker less ticklish rendering easily distinguishable from potentially harmful touches external origin. How brain learns keeps these action-related sensory updated unclear. Here we employ psychophysics functional magnetic resonance imaging pinpoint behavioral neural substrates dynamic recalibration expected temporal delays in self-touch. Our psychophysical results reveal that self-touches are attenuated after systematic exposure delayed self-generated touches, while responses contralateral somatosensory cortex normally distinguish between nondelayed become indistinguishable. During exposure, ipsilateral anterior cerebellum shows increased activity, supporting proposed role recalibrating predictions. Moreover, cingulate areas gradually increase, suggesting as delay adaptation progresses, trigger activity related conflict. Together, our show predictions simplest act upheld sophisticated flexible mechanism maintains accurate time.

Language: Английский

---

Brief Temporal Perturbations in Somatosensory Reafference Disrupt Perceptual and Neural Attenuation and Increase Supplementary Motor Area–Cerebellar Connectivity

Journal of Neuroscience, Journal Year: 2023, Volume and Issue: 43(28), P. 5251 - 5263

Published: June 20, 2023

Intrinsic delays in sensory feedback can be detrimental for motor control. As a compensation strategy, the brain predicts consequences of movement via forward model on basis copy command. Using these predictions, attenuates somatosensory reafference to facilitate processing exafferent information. Theoretically, this predictive attenuation is disrupted by (even minimal) temporal errors between predicted and actual reafference; however, direct evidence such disruption lacking as previous neuroimaging studies contrasted nondelayed reafferent input with input. Here, we combined psychophysics functional magnetic resonance imaging test whether subtle perturbations timing disrupt its processing. Twenty-eight participants (14 women) generated touches their left index finger tapping sensor right finger. The were delivered close time contact two fingers or perturbation (i.e., 153 ms delay). We found that brief at both perceptual neural levels, leading greater cerebellar responses weaker connectivity cerebellum, proportional changes. interpret effects failure predictively attenuate perturbed reafference. Moreover, observed increased supplementary area cerebellum during perturbations, which could indicate communication prediction error back centers. SIGNIFICANCE STATEMENT Our receives from our movements delay. To counteract delays, control theories postulate sensations received time. Thus, self-generated touch feels than an identical external touch. However, how perturb remains unknown. show make otherwise attenuated feel stronger, elicit stronger responses, weaken areas, increase areas. These findings areas are fundamental forming predictions about movements.

Language: Английский

---

Cerebellar Purkinje cells combine sensory and motor information to predict the sensory consequences of active self-motion in macaques

Nature Communications, Journal Year: 2024, Volume and Issue: 15(1)

Published: May 11, 2024

Abstract Accurate perception and behavior rely on distinguishing sensory signals arising from unexpected events those originating our own voluntary actions. In the vestibular system, input that is consequence of active self-motion canceled early at first central stage processing to ensure postural perceptual stability. However, source required cancellation signal was unknown. Here, we show cerebellum combines motor-related information predict consequences self-motion. Recordings during attempted but unrealized head movements in two male rhesus monkeys, revealed encoded by anterior vermis Purkinje cells explain their altered sensitivity versus passive Further, a model combining responses ~40 accounted for observed pathways. These findings establish how cerebellar outcomes self-movements, resolving long-standing issue suppression

Language: Английский

---

Multimodal mismatch responses in mouse auditory cortex

Published: Jan. 28, 2025

Our movements result in predictable sensory feedback that is often multimodal. Based on deviations between predictions and actual input, primary areas of cortex have been shown to compute sensorimotor prediction errors. How errors one modality influence the computation another still unclear. To investigate multimodal mouse auditory (ACx), we used a virtual environment experimentally couple running both self-generated visual feedback. Using two-photon microscopy, first characterized responses layer 2/3 (L2/3) neurons sounds, stimuli, onsets found all three stimuli. Probing evoked by audiomotor mismatches, they closely resemble visuomotor mismatch (V1). Finally, testing for cross modal coupling sound amplitude flow speed running, were amplified when paired with concurrent mismatches. results demonstrate non-hierarchical interactions shape error cortical L2/3.

Language: Английский

---

Multimodal mismatch responses in mouse auditory cortex

eLife, Journal Year: 2025, Volume and Issue: 13

Published: Feb. 10, 2025

Our movements result in predictable sensory feedback that is often multimodal. Based on deviations between predictions and actual input, primary areas of cortex have been shown to compute sensorimotor prediction errors. How errors one modality influence the computation another still unclear. To investigate multimodal mouse auditory cortex, we used a virtual environment experimentally couple running both self-generated visual feedback. Using two-photon microscopy, first characterized responses layer 2/3 (L2/3) neurons sounds, stimuli, onsets found all three stimuli. Probing evoked by audiomotor (AM) mismatches, they closely resemble visuomotor (VM) mismatch (V1). Finally, testing for cross modal AM coupling sound amplitude flow speed running, were amplified when paired with concurrent VM mismatches. results demonstrate non-hierarchical interactions shape error cortical L2/3.

Language: Английский

---