Enhanced modulation of cell-type specific neuronal responses in mouse dorsal auditory field during locomotion

Henschke, Julia U.; Price, Alan T.; Pakan, Janelle M.P.

doi:10.1016/j.ceca.2021.102390

Cited by 18 publications

(21 citation statements)

References 75 publications

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“…Moreover, our large imaging field enabled us to identify a subset of A1 neurons (~1.3% of all imaged neurons) responding specifically to reward consumption and these responses were robust, which is consistent with a previous study reporting licking induced neural activities in a subset A1 neurons (Clayton et al ., 2021). However, these neurons were rare and not a majority of A1 neurons (Francis et al ., 2018) and auditory responses also show heterogeneous modulations by motor signals in A1 (Henschke et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Interactive auditory task reveals complex sensory-action integration in mouse primary auditory cortex

Liu

2022

Preprint

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Predictive coding theory postulates that the brain achieves perception by actively making predictions about the incoming sensory information and correcting them if errors signals arise. These signals are likely the most relevant when the individual is actively interacting with the environment and where the sensory outcome determines the ongoing action. In addition, the cerebral cortex is thought to play a key role in generating these signals. Thus, to study the representation of error signals in the primary sensory cortex, we trained mice to perform an interactive auditory task that coupled their actions to the generated sound and perturbed this coupling to evoke putative error responses. We imaged Layer 2/3 (L2/3) and Layer 4 (L4) neurons in the mouse primary auditory cortex, and we identified not only neurons that mainly encoded action related information but also neurons encoding the mismatch between the action and the sound. These results show that a subset of A1 neurons encode the nonlinear interactions between the sound and the action. Furthermore, more L2/3 neurons encoded action related information than L4, indicating that action-sound integration emerges hierarchically in A1 circuits. Together, our results show that complex interactions between action and sound happen in A1 and that some A1 neurons responses reflect the violation of the learnt relationship between the action and sound feedback. Thus, primary sensory cortices not only encode sensory driven activity but also represent the complex interplay between sensory inputs, expectations, and errors.

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Section: Discussionmentioning

confidence: 99%

Interactive auditory task reveals complex sensory-action integration in mouse primary auditory cortex

Liu

2022

Preprint

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“…This has arisen from the development of advanced microscopy and electrophysiological techniques for recording neural activity while simultaneously probing and manipulating circuit elements ( Dombeck et al, 2007 ; Fois et al, 2014 ; Steinmetz et al, 2021 ). This has enabled neural activity on the network and single-cell level to be directly related to precisely timed stimulus input as well as sequences of ongoing motor behavior (e.g., Gao et al, 2018 ; Pakan et al, 2018a , b ; Musall et al, 2019 ; Henschke et al, 2020 , 2021 ; Dacre et al, 2021 ).…”

Section: Structure and Function Of Distributed Brain Network For Moto...mentioning

confidence: 99%

Engaging distributed cortical and cerebellar networks through motor execution, observation, and imagery

Henschke

Pakan

2023

Front. Syst. Neurosci.

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When we interact with the environment around us, we are sometimes active participants, making directed physical motor movements and other times only mentally engaging with our environment, taking in sensory information and internally planning our next move without directed physical movement. Traditionally, cortical motor regions and key subcortical structures such as the cerebellum have been tightly linked to motor initiation, coordination, and directed motor behavior. However, recent neuroimaging studies have noted the activation of the cerebellum and wider cortical networks specifically during various forms of motor processing, including the observations of actions and mental rehearsal of movements through motor imagery. This phenomenon of cognitive engagement of traditional motor networks raises the question of how these brain regions are involved in the initiation of movement without physical motor output. Here, we will review evidence for distributed brain network activation during motor execution, observation, and imagery in human neuroimaging studies as well as the potential for cerebellar involvement specifically in motor-related cognition. Converging evidence suggests that a common global brain network is involved in both movement execution and motor observation or imagery, with specific task-dependent shifts in these global activation patterns. We will further discuss underlying cross-species anatomical support for these cognitive motor-related functions as well as the role of cerebrocerebellar communication during action observation and motor imagery.

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“…One important concept to explain the role of behavioral state-dependent neural modulation is referred to as 'Active sensation' (Busse et al, 2017;Parker et al, 2020). Essentially, ongoing movement can shape how neurons respond to visual, somatosensory and other sensory stimuli (Chapman et al, 2018;Cruz et al, 2021;Fenk et al, 2021;Fu et al, 2014;Haesemeyer et al, 2018;Henschke et al, 2021). Our data indicate that whole brain activity is elicited with walk onset and maintained afterwards (see Figure 6).…”

Section: Role and Origin Of Broad Activation During Ongoing Behaviormentioning

confidence: 55%

“…Our data suggest that relationships between the activity of neuromodulatory neurons and locomotion are broadly conserved across species. Dopamine neurons are activated during locomotion in mammals, with some neurons reporting ongoing behavior 60 while others are active at behavior onset 61 . We find that although the majority of fly dopamine neurons are activated during ongoing behavior, some dopaminergic neurons are activated milliseconds before the onset of walk (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…One important concept to explain the role of behavioral state-dependent neural modulation is referred to as ‘Active sensation’ (Busse et al, 2017). Essentially, ongoing movement can shape how neurons respond to visual, somatosensory and other sensory stimuli (Chapman et al, 2018; Cruz et al, 2021; Fenk et al, 2021; Henschke et al, 2021; Wolpert et al, 2011). For example, extracellular recordings from V1 neurons of mice walking on a ball showed that evoked visual responses differed during movement as compared to neurons of still animals (Dadarlat and Stryker, 2017).…”

Section: Discussionmentioning

confidence: 99%

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Combined patterns of activity of major neuronal classes underpin a global change in brain state during spontaneous and forced walk inDrosophila

Aimon

Cheng

Gjorgjieva

et al. 2022

Preprint

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Movement and behavioral state influence perception, and a stimulus can elicit opposite behavioral actions depending on whether the animal is moving toward or away from it. Here, we use fast wholebrain lightfield imaging in adult Drosophila melanogaster to analyze the relationship between movement and neuronal activity. Using pan-neuronal calcium imaging, we observe brainwide neuronal activity that tightly correlated with spontaneous bouts of movement. Imaging of specific sets of neurons across the brain reveals that both excitatory and inhibitory as well as different types of neuromodulatory neurons are active during walk inconsistent with a reduction of inhibition on neuronal activity. While most neuron types are activated at walk-onset, serotonergic neurons show more complex patterns of activity with neurons in several brain regions being inhibited during walk. Using available anatomical data, we map forward running and turning-induced activity onto different brain subregions and sometimes individual neurons. Moreover, we find that spontaneous walk and forced walk elicit highly similar wholebrain activity suggesting that a large part of the observed activity corresponds to walk itself rather than its initiation by higher brain centers. Based on our data, we conclude that movement and movement-related sensory feedback signals originating in the ventral nerve cord induce wide-spread activity in the brain allowing the integration of behavioral state into most or all brain processes.

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Enhanced modulation of cell-type specific neuronal responses in mouse dorsal auditory field during locomotion

Cited by 18 publications

References 75 publications

Interactive auditory task reveals complex sensory-action integration in mouse primary auditory cortex

Interactive auditory task reveals complex sensory-action integration in mouse primary auditory cortex

Engaging distributed cortical and cerebellar networks through motor execution, observation, and imagery

Combined patterns of activity of major neuronal classes underpin a global change in brain state during spontaneous and forced walk inDrosophila

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