Stimulation of the subparafascicular thalamic nucleus modulates dopamine release in the inferior colliculus of rats

Batton, Aiyana D.; Blaha, Charles D.; Bieber, Allan J.; Lee, Kendall H.; Boschen, Suelen Lúcio

doi:10.1002/syn.22073

Cited by 11 publications

(17 citation statements)

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“…Hence, these signed "reward PEs" encoded by dopaminergic neurons are substantially different from the unsigned "sensory PEs" encoded by auditory neurons in the nonlemniscal IC [31][32][33]. According to this classic interpretation of dopaminergic PLOS BIOLOGY function, exogenous dopamine ejections in the nonlemniscal IC should mimic reinforcing signals coming from the SPF [51][52][53][54][55]57]. Speculatively, such dopaminergic input might aim to induce long-term potentiation on IC neurons to build lasting associations between acoustic cues and rewarding outcomes, thereby contributing to establish reward expectations.…”

Section: Spf Dopaminergic Projections To the Ic Could Scale Sensory Pesmentioning

confidence: 99%

“…On the other hand, dopamine and eticlopride can interact with D 2 -like receptors expressed in a presynaptic neuron. Both glutamatergic and GABAergic projections converge onto single IC neurons [49,71,72], which may also receive dopaminergic inputs from the SPF [51][52][53][54][55]57]. Dopamine could potentially activate presynaptic D 2 -like receptors expressed in a excitatory neuron, as described in striatal medium spiny neurons [73][74][75], or conversely in a inhibitory neuron, as demonstrated in the ventral tegmental area [76].…”

Section: Intrinsic and Synaptic Properties Generate Heterogeneous Dopmentioning

confidence: 99%

“…As a result, the otherwise irreducible PE prompted by oddball stimuli can be minimized from a rather early stage of auditory processing. In natural conditions, such midbrain-level scaling of PEs could be performed by SPF dopaminergic neurons projecting to the IC [51][52][53][54][55][56][57][58]. Both glutamatergic and GABAergic neurons in the nonlemniscal IC receive comparable dopaminergic innervation from the SPF [55].…”

Section: Plos Biologymentioning

confidence: 99%

“…As a site of convergence of both ascending and descending auditory pathways, the IC plays a key role in processing surprising sounds [47] and shaping the auditory context [48]. The complex computational network of the IC integrates excitatory, inhibitory, and rich neuromodulatory input [49,50], which includes dopaminergic innervation from the thalamic subparafascicular nucleus (SPF) [51][52][53][54][55][56][57][58]. Previous reports have detected mRNA coding for dopaminergic D 2 -like receptors in the IC [57,58] and proved its functional expression as protein.…”

Section: Introductionmentioning

confidence: 99%

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Dopamine modulates subcortical responses to surprising sounds

et al. 2020

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Dopamine guides behavior and learning through pleasure, according to classic understanding. Dopaminergic neurons are traditionally thought to signal positive or negative prediction errors (PEs) when reward expectations are, respectively, exceeded or not matched. These signed PEs are quite different from the unsigned PEs, which report surprise during sensory processing. But mounting theoretical accounts from the predictive processing framework postulate that dopamine, as a neuromodulator, could potentially regulate the postsynaptic gain of sensory neurons, thereby scaling unsigned PEs according to their expected precision or confidence. Despite ample modeling work, the physiological effects of dopamine on the processing of surprising sensory information are yet to be addressed experimentally. In this study, we tested how dopamine modulates midbrain processing of unexpected tones. We recorded extracellular responses from the rat inferior colliculus to oddball and cascade sequences, before, during, and after the microiontophoretic application of dopamine or eticlopride (a D 2-like receptor antagonist). Results demonstrate that dopamine reduces the net neuronal responsiveness exclusively to unexpected sensory input without significantly altering the processing of expected input. We conclude that dopaminergic projections from the thalamic subparafascicular nucleus to the inferior colliculus could encode the expected precision of unsigned PEs, attenuating via D 2-like receptors the postsynaptic gain of sensory inputs forwarded by the auditory midbrain neurons. This direct dopaminergic modulation of sensory PE signaling has profound implications for both the predictive coding framework and the understanding of dopamine function.

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Section: Spf Dopaminergic Projections To the Ic Could Scale Sensory Pesmentioning

confidence: 99%

Section: Intrinsic and Synaptic Properties Generate Heterogeneous Dopmentioning

confidence: 99%

Section: Plos Biologymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Dopamine modulates subcortical responses to surprising sounds

et al. 2020

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“…In natural conditions, such midbrain-level gating of prediction errors could be shaped by SPF dopaminergic neurons projecting to the cortices of the IC [11,35,48]. Many auditory nuclei project to the SPF, including auditory cortex, auditory thalamus, the IC and the superior olivary complex, providing it with rich auditory information [48–52].…”

Section: Discussionmentioning

confidence: 99%

Dopamine modulates prediction error forwarding in the nonlemniscal inferior colliculus

Valdés-Baizabal

Carbajal

Pérez-González

et al. 2019

Preprint

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Short title: Dopamine gates prediction error forwarding in the IC cortices 14 15 Keywords: inferior colliculus (IC), stimulus-specific adaptation (SSA), predictive coding, 16 prediction error, precision, dopamine, auditory 17 18 Highlights 19• Dopamine reduces the responsiveness of IC neurons to unexpected 20 sounds exclusively. 21• Dopamine decreases prediction error forwarding from the IC cortices. 22• Dopaminergic input to the IC cortices encodes precision of prediction 23 errors. 24 Abstract 25 Predictive coding theory describes perception as a hierarchical predictive model 26 of sensation. Higher-level neural structures constrain the processing at lower-27 level structures by suppressing synaptic activity induced by predictable sensory 28 input. But when predictions fail, deviant input is forwarded bottom-up as 29 'prediction error' to update the perceptual model. The earliest prediction error 30 signals identified in the auditory pathway emerge from the cortices of the inferior 31 colliculus (IC). The drive that each prediction error has on the perceptual model 32 depends on its 'precision', which is theoretically encoded by the dopaminergic 33 system. To test it empirically, we recorded single-unit responses from the rat IC 34 cortices to oddball and cascade sequences before, during and after the 35 microiontophoretic application of dopamine or eticlopride (a D2-like receptor 36 antagonist). Thereby, we studied dopaminergic modulation on the subcortical 37 processing of unpredictable and predictable auditory changes. Results 38 demonstrate that dopamine reduces neuronal responsiveness exclusively to 39 unexpected auditory input. High dopamine concentrations in the neuronal 40 microdomain reduce prediction error forwarding via D2-like receptors, without 41 significantly altering repetition suppression. Thus, already at subcortical levels of 42 the auditory pathway, dopaminergic input to the IC gates the bottom-up flow of 43 prediction error signals by encoding their precision.44 45 46 47 48 49 List of abbreviatures 50 CAS: deviant condition. 51 CSI: common SSA index. 52 dB SPL: decibels sound pressure level. 53 DEV: deviant condition. 54 FRA: frequency response area. 55 IC: inferior colliculus. 56 iMM: index of neuronal mismatch. 57 iPE: index of prediction error. 58 iRS: index of repetition suppression. 59 mRNA: messenger RNA 60 PSTH: peristimulus time histogram. 61 SPF: subparafascicular nucleus of the thalamus. 62 SSA: stimulus-specific adaptation. 63 STD: standard condition. 64 TDT: Tucker-Davis Technologies. 65 66 67 68 69 70 71 72Perceptual systems prune redundant sensory input as a means of sparing 73 processing resources while providing saliency to input that is rare, unique, and 74 therefore potentially more informative. This perceptual function has been 75 classically studied in humans using the auditory oddball paradigm (Fig. 1A) [1], 76 where the successive repetition of a tone ('standard condition', henceforth 'STD') 77 is randomly interrupted by an 'oddball' tone ('deviant condition', hence...

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Dopamine in the Auditory System of Vocal Toadfishes: Potential Adaptation for Noisy Aquatic Environments

Hom

Forlano

2023

The Effects of Noise on Aquatic Life

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Stimulation of the subparafascicular thalamic nucleus modulates dopamine release in the inferior colliculus of rats

Cited by 11 publications

References 53 publications

Dopamine modulates subcortical responses to surprising sounds

Dopamine modulates subcortical responses to surprising sounds

Dopamine modulates prediction error forwarding in the nonlemniscal inferior colliculus

Dopamine in the Auditory System of Vocal Toadfishes: Potential Adaptation for Noisy Aquatic Environments

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