Locomotion and Task Demands Differentially Modulate Thalamic Audiovisual Processing during Active Search

Abstract

SUMMARY Active search is a ubiquitous goal-driven behavior wherein organisms purposefully investigate the sensory environment to locate a target object. During active search, brain circuits analyze a stream of sensory information from the external environment, adjusting for internal signals related to self-generated movement or “top-down” weighting of anticipated target and distractor properties. Sensory responses in the cortex can be modulated by internal state [1–9], though the extent and form of modulation arising in the cortex de novo versus an inheritance from subcortical stations is not clear [4, 8–12]. We addressed this question by simultaneously recording from auditory and visual regions of the thalamus (MG and LG, respectively) while mice used dynamic auditory or visual feedback to search for a hidden target within an annular track. Locomotion was associated with strongly suppressed responses and reduced decoding accuracy in MG but a subtle increase in LG spiking. Because stimuli in one modality provided critical information about target location while the other served as a distractor, we could also estimate the importance of task relevance in both thalamic subdivisions. In contrast to the effects of locomotion, we found that LG responses were reduced overall yet decoded stimuli more accurately when vision was behaviorally relevant, whereas task relevance had little effect on MG responses. This double dissociation between the influences of task relevance and movement in MG and LG highlights a role for extrasensory modulation in the thalamus but also suggests key differences in the organization of modulatory circuitry between the auditory and visual pathways.

Basal forebrain contributes to default mode network regulation

“…6A, Right)]. However, we did observe enhanced high gamma activity between 60 and 100 Hz during arena exploration (paired t test: P < 10 −8 ), which we attribute to previously described VC activation during locomotion (39,40). To explore the functional coupling of the two cortical areas with the BF, we computed coherence spectra (Fig.…”

Audiomotor Perceptual Training Enhances Speech Intelligibility in Background Noise

“…The difficulty level of the task adaptively changed such that advancing to later puzzle boards imposed higher memory loads, longer delay periods, and additional distractor elements (Figure 1B, middle and bottom ). The CL audiomotor training task was modeled after earlier work on CL training tasks in animal [30–32,44] and human [30] subjects. In brief, subjects discriminated subtle changes in continuous auditory feedback to trace the outline of the hidden puzzle piece (Figure 1C, top ), place the puzzle piece in its correct position within the puzzle board (Figure S4A–C), and then rotate the piece into the correct orientation (Figure S4G–I).…”

Motor-related signals in the auditory system for listening and learning

“…In fact, recent studies using intracellular and extracellular recording combined with optogenetic methods in freely behaving mice provide evidence that movement-related signals actively suppress auditory cortical activity through a combination of mechanisms including increased activity in local inhibitory circuits 22 and decreased excitatory drive from the thalamus 24 and from within the auditory cortex 23 .…”

“…Although local inhibition accounts for decreased responsiveness to acoustic stimuli within the auditory cortex, withdrawal of excitatory drive from the auditory thalamus may also play a role in suppressing auditory cortex during movement 24 . To distinguish the relative contributions of cortical and subcortical suppression, Schneider et al used an optogenetic approach to selectively activate auditory thalamic inputs to the cortex and compared how movement affected cortical responses to thalamic terminal activation, which are likely to be influenced only by movement-related signals acting in the cortex, and to tones, which are potentially influenced by movement-related signals acting at many sites along the auditory neuraxis.…”

“…Alternatively, auditory cortical sensitivity could actually increase if spontaneous firing rates decrease more than tone-evoked firing rates during movement, resulting in an increased signal-to-noise ratio 23 . In fact, such a boost in signal-to-noise ratios occurs in the auditory cortex of rodents performing auditory discrimination tasks that require attention 24,27 , suggesting that this mechanism may also be exploited during movement. Additionally, movement-related suppression in the mouse auditory cortex may reflect a predictive mechanism that facilitates the distinction between reafferent and exafferent sounds, as has been described in the auditory cortex of vocalizing primates 1 .…”