Predictive Filtering of Sensory Response Via Orbitofrontal Top-down Input

Overview

Journal bioRxiv

Date 2024 Sep 30

PMID 39345607

Authors

Hiroaki Tsukano

Michellee M Garcia

Michellee Marie Garcia

Pranathi R Dandu

Pranathi Reddy Dandu

Hiroyuki K Kato

Affiliations

Soon will be listed here.

Abstract

Habituation is a crucial sensory filtering mechanism whose dysregulation can lead to a continuously intense world in disorders with sensory overload. While habituation is considered to require top-down predictive signaling to suppress irrelevant inputs, the exact brain loci storing the internal predictive model and the circuit mechanisms of sensory filtering remain unclear. We found that daily neural habituation in the primary auditory cortex (A1) was reversed by inactivation of the orbitofrontal cortex (OFC). Top-down projections from the ventrolateral OFC, but not other frontal areas, carried predictive signals that grew with daily sound experience and suppressed A1 via somatostatin-expressing inhibitory neurons. Thus, prediction signals from the OFC cancel out behaviorally irrelevant anticipated stimuli by generating their "negative images" in sensory cortices.

References

Wehr M, Zador A . Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron. 2005; 47(3):437-45. DOI: 10.1016/j.neuron.2005.06.009. View

Anderson L, Christianson G, Linden J . Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci. 2009; 29(22):7359-63. PMC: 6666468. DOI: 10.1523/JNEUROSCI.0793-09.2009. View

Jamal W, Cardinaux A, Haskins A, Kjelgaard M, Sinha P . Reduced Sensory Habituation in Autism and Its Correlation with Behavioral Measures. J Autism Dev Disord. 2020; 51(9):3153-3164. DOI: 10.1007/s10803-020-04780-1. View

Namboodiri V, Otis J, van Heeswijk K, Voets E, Alghorazi R, Rodriguez-Romaguera J . Single-cell activity tracking reveals that orbitofrontal neurons acquire and maintain a long-term memory to guide behavioral adaptation. Nat Neurosci. 2019; 22(7):1110-1121. PMC: 7002110. DOI: 10.1038/s41593-019-0408-1. View

Dissegna A, Turatto M, Chiandetti C . Context-Specific Habituation: A Review. Animals (Basel). 2021; 11(6). PMC: 8231551. DOI: 10.3390/ani11061767. View

Whyte A, Kietzman H, Swanson A, Butkovich L, Barbee B, Bassell G . Reward-Related Expectations Trigger Dendritic Spine Plasticity in the Mouse Ventrolateral Orbitofrontal Cortex. J Neurosci. 2019; 39(23):4595-4605. PMC: 6554633. DOI: 10.1523/JNEUROSCI.2031-18.2019. View

Jiang X, Shen S, Cadwell C, Berens P, Sinz F, Ecker A . Principles of connectivity among morphologically defined cell types in adult neocortex. Science. 2015; 350(6264):aac9462. PMC: 4809866. DOI: 10.1126/science.aac9462. View

Senzai Y, Fernandez-Ruiz A, Buzsaki G . Layer-Specific Physiological Features and Interlaminar Interactions in the Primary Visual Cortex of the Mouse. Neuron. 2019; 101(3):500-513.e5. PMC: 6367010. DOI: 10.1016/j.neuron.2018.12.009. View

Natan R, Briguglio J, Mwilambwe-Tshilobo L, Jones S, Aizenberg M, Goldberg E . Complementary control of sensory adaptation by two types of cortical interneurons. Elife. 2015; 4. PMC: 4641469. DOI: 10.7554/eLife.09868. View

10.

Gottfried J, ODoherty J, Dolan R . Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science. 2003; 301(5636):1104-7. DOI: 10.1126/science.1087919. View

11.

Vissers M, Cohen M, Geurts H . Brain connectivity and high functioning autism: a promising path of research that needs refined models, methodological convergence, and stronger behavioral links. Neurosci Biobehav Rev. 2011; 36(1):604-25. DOI: 10.1016/j.neubiorev.2011.09.003. View

12.

Costa K, Scholz R, Lloyd K, Moreno-Castilla P, Gardner M, Dayan P . The role of the lateral orbitofrontal cortex in creating cognitive maps. Nat Neurosci. 2022; 26(1):107-115. PMC: 9839657. DOI: 10.1038/s41593-022-01216-0. View

13.

Wass S . Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn. 2010; 75(1):18-28. DOI: 10.1016/j.bandc.2010.10.005. View

14.

Ying R, Hamlette L, Nikoobakht L, Balaji R, Miko N, Caras M . Organization of orbitofrontal-auditory pathways in the Mongolian gerbil. J Comp Neurol. 2023; 531(14):1459-1481. PMC: 10529810. DOI: 10.1002/cne.25525. View

15.

Wilson R, Takahashi Y, Schoenbaum G, Niv Y . Orbitofrontal cortex as a cognitive map of task space. Neuron. 2014; 81(2):267-279. PMC: 4001869. DOI: 10.1016/j.neuron.2013.11.005. View

16.

Sun W, Tang P, Liang Y, Li J, Feng J, Zhang N . The anterior cingulate cortex directly enhances auditory cortical responses in air-puffing-facilitated flight behavior. Cell Rep. 2022; 38(10):110506. DOI: 10.1016/j.celrep.2022.110506. View

17.

Nyiri G, Stephenson F, Freund T, Somogyi P . Large variability in synaptic N-methyl-D-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus. Neuroscience. 2003; 119(2):347-63. DOI: 10.1016/s0306-4522(03)00157-x. View

18.

Kato H, Gillet S, Isaacson J . Flexible Sensory Representations in Auditory Cortex Driven by Behavioral Relevance. Neuron. 2015; 88(5):1027-1039. PMC: 4670799. DOI: 10.1016/j.neuron.2015.10.024. View

19.

Makino H, Komiyama T . Learning enhances the relative impact of top-down processing in the visual cortex. Nat Neurosci. 2015; 18(8):1116-22. PMC: 4523093. DOI: 10.1038/nn.4061. View

20.

Schoenbaum G, Roesch M, Stalnaker T, Takahashi Y . A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat Rev Neurosci. 2009; 10(12):885-92. PMC: 2835299. DOI: 10.1038/nrn2753. View