Cooperative thalamocortical circuit mechanism for sensory prediction errors DOI Open Access

Shohei Furutachi,

Alexis D. Franklin, Thomas D. Mrsic‐Flogel

et al.

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

Untangling the cortico-thalamo-cortical loop: cellular pieces of a knotty circuit puzzle DOI
Gordon M. Shepherd, Naoki Yamawaki

Nature reviews. Neuroscience, Journal Year: 2021, Volume and Issue: 22(7), P. 389 - 406

Published: May 6, 2021

Language: Английский

Citations

188
Cortical somatostatin interneuron subtypes form cell-type-specific circuits DOI
Jingjing Sherry Wu, Elaine Sevier, Deepanjali Dwivedi

et al.

Neuron, Journal Year: 2023, Volume and Issue: 111(17), P. 2675 - 2692.e9

Published: June 29, 2023

Language: Английский

Citations

73
Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep DOI Open Access
Mattia Aime, Niccolò Calcini, Micaela Borsa

et al.

Science, Journal Year: 2022, Volume and Issue: 376(6594), P. 724 - 730

Published: May 12, 2022

Rapid eye movement (REM) sleep is associated with the consolidation of emotional memories. Yet, underlying neocortical circuits and synaptic mechanisms remain unclear. We found that REM a somatodendritic decoupling in pyramidal neurons prefrontal cortex. This reflects shift inhibitory balance between parvalbumin neuron-mediated somatic inhibition vasoactive intestinal peptide-mediated dendritic disinhibition, mostly driven by from central medial thalamus. REM-specific optogenetic suppression activity led to loss danger-versus-safety discrimination during associative learning lack plasticity, whereas release resulted enhanced potentiation. Somatodendritic promotes opposite plasticity optimize responses future behavioral stressors.

Language: Английский

Citations

72
Cooperative thalamocortical circuit mechanism for sensory prediction errors DOI Creative Commons

Shohei Furutachi,

Alexis D. Franklin, Andreea M. Aldea

et al.

Nature, Journal Year: 2024, Volume and Issue: 633(8029), P. 398 - 406

Published: Aug. 28, 2024

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 prediction-error signals for various neural computations across brain, surprisingly little is known about circuit mechanisms responsible their implementation. Here we describe thalamocortical disinhibitory that required generating sensory in mouse primary visual cortex (V1). We show violating animals’ predictions by stimulus preferentially boosts responses layer 2/3 V1 neurons most selective stimulus. Prediction errors specifically amplify input, rather than representing non-specific surprise or difference how input deviates from animal’s predictions. This amplification implemented cooperative mechanism requiring thalamic pulvinar cortical vasoactive-intestinal-peptide-expressing (VIP) inhibitory interneurons. In response VIP inhibit specific subpopulation somatostatin-expressing interneurons gate excitatory V1, resulting pulvinar-driven stimulus-selective V1. Therefore, prioritizes unpredicted information selectively increasing salience features through synergistic interaction neocortical circuits.

Language: Английский

Citations

16
Anatomically and functionally distinct thalamocortical inputs to primary and secondary mouse whisker somatosensory cortices DOI Creative Commons
Sami El Boustani, B. Semihcan Sermet, Georgios Foustoukos

et al.

Nature Communications, Journal Year: 2020, Volume and Issue: 11(1)

Published: July 3, 2020

Abstract Subdivisions of mouse whisker somatosensory thalamus project to cortex in a region-specific and layer-specific manner. However, clear anatomical dissection these pathways their functional properties during sensation is lacking. Here, we use anterograde trans-synaptic viral vectors identify three specific thalamic subpopulations based on connectivity with brainstem. The principal trigeminal nucleus innervates ventral posterior medial thalamus, which conveys whisker-selective tactile information layer 4 primary that highly sensitive self-initiated movements. spinal rostral part the (POm) signaling sensory information, as well decision-related goal-directed behavior, secondary cortex. A caudal POm, apparently does not receive brainstem input, 1 5A, responding little selectivity, but showing modulation. Our results suggest existence complementary segregated streams cortices.

Language: Английский

Citations

120
Neuronal Circuits in Barrel Cortex for Whisker Sensory Perception DOI
Jochen F. Staiger, Carl C.H. Petersen

Physiological Reviews, Journal Year: 2020, Volume and Issue: 101(1), P. 353 - 415

Published: Aug. 20, 2020

The array of whiskers on the snout provides rodents with tactile sensory information relating to size, shape and texture objects in their immediate environment. Rodents can use detect stimuli, distinguish textures, locate navigate. Important aspects whisker sensation are thought result from neuronal computations somatosensory cortex (wS1). Each is individually represented somatotopic map wS1 by an anatomical unit named a ‘barrel’ (hence also called barrel cortex). This allows precise investigation processing context well-defined map. Here, we first review signaling pathways wS1, then discuss current understanding various types excitatory inhibitory neurons present within wS1. Different classes cells be defined according anatomical, electrophysiological molecular features. synaptic connectivity local microcircuits, as well long-range interactions impact neuromodulators, beginning understood. Recent technological progress has allowed cell-type-specific related activity during whisker-related behaviors. An important goal for future research obtain causal mechanistic how selected processed specific synaptically connected networks signaled downstream brain areas, thus contributing sensory-guided decision-making.

Language: Английский

Citations

113
Sensory input drives rapid homeostatic scaling of the axon initial segment in mouse barrel cortex DOI Creative Commons
Nora Jamann, Dominik Dannehl, Nadja Lehmann

et al.

Nature Communications, Journal Year: 2021, Volume and Issue: 12(1)

Published: Jan. 4, 2021

Abstract The axon initial segment (AIS) is a critical microdomain for action potential initiation and implicated in the regulation of neuronal excitability during activity-dependent plasticity. While structural AIS plasticity has been suggested to fine-tune activity when network states change, whether it acts vivo as homeostatic regulatory mechanism behaviorally relevant contexts remains poorly understood. Using mouse whisker-to-barrel pathway model system combination with immunofluorescence, confocal analysis electrophysiological recordings, we observed bidirectional cortical pyramidal neurons. Furthermore, find that functional remodeling occurs distinct temporal domains: Long-term sensory deprivation elicits an length increase, accompanied increase excitability, while enrichment results rapid shortening, by decrease generation. Our findings highlight central role input-output relations.

Language: Английский

Citations

83
Cell-type-specific recruitment of GABAergic interneurons in the primary somatosensory cortex by long-range inputs DOI Creative Commons
Shovan Naskar, Jia Qi, Francisco Pereira

et al.

Cell Reports, Journal Year: 2021, Volume and Issue: 34(8), P. 108774 - 108774

Published: Feb. 1, 2021

Extensive hierarchical yet highly reciprocal interactions among cortical areas are fundamental for information processing. However, connectivity rules governing the specificity of such corticocortical connections, and top-down feedback projections in particular, poorly understood. We analyze synaptic strength from functionally relevant brain to diverse neuronal types primary somatosensory cortex (S1). Long-range different preferentially engage specific sets GABAergic neurons S1. Projections other cortices strongly recruit parvalbumin (PV)-positive lead PV neuron-mediated feedforward inhibition pyramidal In contrast, inputs whisker-related motor biased vasoactive intestinal peptide (VIP)-positive potentially result VIP disinhibition. Regardless input areas, somatostatin-positive receive relatively weak long-range inputs. Computational analyses suggest that a characteristic combination IN S1 represents area.

Language: Английский

Citations

66
Precise movement-based predictions in the mouse auditory cortex DOI Creative Commons
Nicholas J. Audette, Wenxi Zhou, Alessandro La Chioma

et al.

Current Biology, Journal Year: 2022, Volume and Issue: 32(22), P. 4925 - 4940.e6

Published: Oct. 24, 2022

Language: Английский

Citations

48
Thalamic bursting and the role of timing and synchrony in thalamocortical signaling in the awake mouse DOI Creative Commons
Peter Y. Borden, Nathaniel C. Wright, Arthur E. Morrissette

et al.

Neuron, Journal Year: 2022, Volume and Issue: 110(17), P. 2836 - 2853.e8

Published: July 7, 2022

Language: Английский

Citations

41