Auditory input enhances somatosensory encoding and tactile goal-directed behavior.
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ABSTRACT:
SUBMITTER: Godenzini L
PROVIDER: S-EPMC8302566 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:To synthesize a coherent representation of the external world, the brain must integrate inputs across different types of stimuli. Yet the mechanistic basis of this computation at the level of neuronal populations remains obscure. Here, we investigate tactile-auditory integration using two-photon Ca2+ imaging in the mouse primary (S1) and secondary (S2) somatosensory cortices. Pairing sound with whisker stimulation modulates tactile responses in both S1 and S2, with the most prominent modulation being robust inhibition in S2. The degree of inhibition depends on tactile stimulation frequency, with lower frequency responses the most severely attenuated. Alongside these neurons, we identify sound-selective neurons in S2 whose responses are inhibited by high tactile frequencies. These results are consistent with a hypothesized local mutually-inhibitory S2 circuit that spectrally selects tactile versus auditory inputs. Our findings enrich mechanistic understanding of multisensory integration and suggest a key role for S2 in combining auditory and tactile information.
| S-EPMC7012892 | biostudies-literature
Project description:Prompt execution of planned motor action is essential for survival. The interactions between frontal cortical circuits and the basal ganglia are central to goal-oriented action selection and initiation.1-4 In rodents, the ventromedial thalamic nucleus (VM) is one of the critical nodes that conveys the output of the basal ganglia to the frontal cortical areas including the anterior lateral motor cortex (ALM).5-9 Recent studies showed the critical role of ALM and its interplay with the motor thalamus in preparing sensory-cued rewarded movements, specifically licking.10-12 Work in primates suggests that the basal ganglia output to the motor thalamus transmits an urgency or vigor signal,13-15 which leads to shortened reaction times and faster movement initiation. As yet, little is known about what signals are transmitted from the motor thalamus to the cortex during cued movements and how these signals contribute to movement initiation. In the present study, we employed a tactile-cued licking task in mice while monitoring reaction times of the initial lick. We found that inactivation of ALM delayed the initiation of cued licking. Two-photon Ca2+ imaging of VM axons revealed that the majority of the axon terminals in ALM were transiently active during licking. Their activity was predictive of the time of the first lick. Chemogenetic and optogenetic manipulation of VM axons in ALM indicated that VM inputs facilitate the initiation of cue-triggered and impulsive licking in trained mice. Our results suggest that VM thalamocortical inputs increase the probability and vigor of initiating planned motor responses.
| S-EPMC8478854 | biostudies-literature
Project description:BackgroundCognitive inflexibility is a core symptom of several mental disorders including schizophrenia. Brain imaging studies in schizophrenia patients performing cognitive tasks have reported decreased activation of the mediodorsal thalamus (MD). Using a pharmacogenetic approach to model MD hypofunction, we recently showed that decreasing MD activity impairs reversal learning in mice. While this demonstrates causality between MD hypofunction and cognitive inflexibility, questions remain about the elementary cognitive processes that account for the deficit.MethodsUsing the Designer Receptors Exclusively Activated by Designer Drugs system, we reversibly decreased MD activity during behavioral tasks assessing elementary cognitive processes inherent to flexible goal-directed behaviors, including extinction, contingency degradation, outcome devaluation, and Pavlovian-to-instrumental transfer (n = 134 mice).ResultsWhile MD hypofunction impaired reversal learning, it did not affect the ability to learn about nonrewarded cues or the ability to modulate action selection based on the outcome value. In contrast, decreasing MD activity delayed the ability to adapt to changes in the contingency between actions and their outcomes. In addition, while Pavlovian learning was not affected by MD hypofunction, decreasing MD activity during Pavlovian learning impaired the ability of conditioned stimuli to modulate instrumental behavior.ConclusionsMediodorsal thalamus hypofunction causes cognitive inflexibility reflected by an impaired ability to adapt actions when their consequences change. Furthermore, it alters the encoding of environmental stimuli so that they cannot be properly utilized to guide behavior. Modulating MD activity could be a potential therapeutic strategy for promoting adaptive behavior in human subjects with cognitive inflexibility.
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Project description:BackgroundAttentional processes are modulated by current goal pursuit. While pursuing salient cognitive goals, individuals prioritize goal-related information and suppress goal-irrelevant ones. This occurs in the context of pain too, where nonpain cognitive goal pursuit was found to have inhibitory effects on pain-related attention. Crucially, how pursuing nonpain motor goals affects pain-related somatosensory attention is still unknown. The aim of this study was to investigate whether nonpain motor goal pursuit would attenuate pain-related somatosensory attention.MethodsHealthy volunteers (N = 45) performed a robotic arm conditioning task where movements were paired with conflicting (pain and reward), threatening (only pain) or neutral (no pain and no reward) outcomes. To increase the motivational value of pursuing the nonpain motor goal, in the conflicting condition participants could receive a reward for a good motor performance. To examine somatosensory attention during movement, somatosensory evoked potentials (SEPs; N120 and P200) were obtained in response to innocuous tactile stimuli administered on a pain-relevant or pain-irrelevant body location. We expected that the threat of pain would enhance somatosensory attention. Furthermore, we expected that the possibility of getting a reward would inhibit this effect, due to pain-reward interactions.ResultsAgainst our predictions, the amplitude of the N120 did not differ across movement types and locations. Furthermore, the P200 component showed significantly larger SEPs for conflicting and threat movements compared to neutral, suggesting that the threat of pain increased somatosensory attention. However, this effect was not modulated by nonpain motor goal pursuit, as reflected by the lack of modulation of the N120 and P200 in the conflicting condition as compared to the threat condition. This study corroborates the idea that pain-related somatosensory attention is enhanced by threat of pain, even when participants were motivated to move to obtain a reward.
| S-EPMC10748472 | biostudies-literature
Project description:The acts of learning and memory are thought to emerge from the modifications of synaptic connections between neurons, as guided by sensory feedback during behavior. However, much is unknown about how such synaptic processes can sculpt and are sculpted by neuronal population dynamics and an interaction with the environment. Here, we embodied a simulated network, inspired by dissociated cortical neuronal cultures, with an artificial animal (an animat) through a sensory-motor loop consisting of structured stimuli, detailed activity metrics incorporating spatial information, and an adaptive training algorithm that takes advantage of spike timing dependent plasticity. By using our design, we demonstrated that the network was capable of learning associations between multiple sensory inputs and motor outputs, and the animat was able to adapt to a new sensory mapping to restore its goal behavior: move toward and stay within a user-defined area. We further showed that successful learning required proper selections of stimuli to encode sensory inputs and a variety of training stimuli with adaptive selection contingent on the animat's behavior. We also found that an individual network had the flexibility to achieve different multi-task goals, and the same goal behavior could be exhibited with different sets of network synaptic strengths. While lacking the characteristic layered structure of in vivo cortical tissue, the biologically inspired simulated networks could tune their activity in behaviorally relevant manners, demonstrating that leaky integrate-and-fire neural networks have an innate ability to process information. This closed-loop hybrid system is a useful tool to study the network properties intermediating synaptic plasticity and behavioral adaptation. The training algorithm provides a stepping stone towards designing future control systems, whether with artificial neural networks or biological animats themselves.
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Project description:This study examined the trainability of the proprioceptive sense and explored the relationship between proprioception and motor learning. With vision blocked, human learners had to perform goal-directed wrist movements relying solely on proprioceptive/haptic cues to reach several haptically specified targets. One group received additional somatosensory movement error feedback in form of vibro-tactile cues applied to the skin of the forearm. We used a haptic robotic device for the wrist and implemented a 3-day training regimen that required learners to make spatially precise goal-directed wrist reaching movements without vision. We assessed whether training improved the acuity of the wrist joint position sense. In addition, we checked if sensory learning generalized to the motor domain and improved spatial precision of wrist tracking movements that were not trained. The main findings of the study are: First, proprioceptive acuity of the wrist joint position sense improved after training for the group that received the combined proprioceptive/haptic and vibro-tactile feedback (VTF). Second, training had no impact on the spatial accuracy of the untrained tracking task. However, learners who had received VTF significantly reduced their reliance on haptic guidance feedback when performing the untrained motor task. That is, concurrent VTF was highly salient movement feedback and obviated the need for haptic feedback. Third, VTF can be also provided by the limb not involved in the task. Learners who received VTF to the contralateral limb equally benefitted. In conclusion, somatosensory training can significantly enhance proprioceptive acuity within days when learning is coupled with vibro-tactile sensory cues that provide feedback about movement errors. The observable sensory improvements in proprioception facilitates motor learning and such learning may generalize to the sensorimotor control of the untrained motor tasks. The implications of these findings for neurorehabilitation are discussed.
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Project description:When pursuing high-value goals, mature individuals typically titrate cognitive performance according to environmental demands. However, it remains unclear whether adolescents similarly integrate value-based goals to selectively enhance goal-directed behavior. We used a value-contingent cognitive control task during fMRI to assess how stakes-the value of a prospective outcome-modulate flexible goal-directed behavior and underlying neurocognitive processes. Here we demonstrate that while adults enhance performance during high stakes, adolescents perform similarly during low and high stakes conditions. The developmental emergence of value-contingent performance is mediated by connectivity between the striatum and prefrontal cortex; this connectivity selectively increases during high stakes and with age. These findings suggest that adolescents may not benefit from high stakes to the same degree adults do-a behavioral profile that may be constrained by ongoing maturation of corticostriatal connectivity. We propose that late development of corticostriatal connectivity sets the stage for optimal goal-directed behavior.
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Project description:The prefrontal cortex (PFC) plays a key role in controlling goal-directed behavior. Although a variety of task-related signals have been observed in the PFC, whether they are differentially encoded by various cell types remains unclear. Here we performed cellular-resolution microendoscopic Ca(2+) imaging from genetically defined cell types in the dorsomedial PFC of mice performing a PFC-dependent sensory discrimination task. We found that inhibitory interneurons of the same subtype were similar to each other, but different subtypes preferentially signaled different task-related events: somatostatin-positive neurons primarily signaled motor action (licking), vasoactive intestinal peptide-positive neurons responded strongly to action outcomes, whereas parvalbumin-positive neurons were less selective, responding to sensory cues, motor action, and trial outcomes. Compared to each interneuron subtype, pyramidal neurons showed much greater functional heterogeneity, and their responses varied across cortical layers. Such cell-type and laminar differences in neuronal functional properties may be crucial for local computation within the PFC microcircuit.
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