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Awake delta and theta-rhythmic hippocampal network modes during intermittent locomotor behaviors in the rat.

ABSTRACT: Delta-frequency network activity is commonly associated with sleep or behavioral disengagement accompanied by a dearth of cortical spiking, but delta in awake behaving animals is not well understood. We show that hippocampal (HC) synchronization in the delta frequency band (1-4 Hz) is related to animals' locomotor behavior using detailed analyses of the HC local field potential (LFP) and simultaneous head- and body-tracking data. In contrast to running-speed modulation of the theta rhythm (6-10 Hz), delta was most prominent when animals were stationary or moving slowly, that is, when theta and fast gamma (65-120 Hz) were weak, and often developed rapidly when animals paused briefly between runs. We next combined time-frequency decomposition of the LFP with hierarchical clustering algorithms to categorize momentary estimations of the power spectral density (PSD) into putative modes of HC activity. Delta and theta power were strikingly orthogonal across spectral modes, as well as across bouts of precisely defined running and stationary behavior. Delta-band and theta-band coherences between HC recording sites were monotonically related to theta-delta ratios across modes; and whereas theta coherence between HC and medial prefrontal cortex (mPFC) increased during running, delta-band coherence between mPFC and HC increased during stationary bouts. Taken together, our findings suggest that delta-dominated network modes (and corresponding mPFC-HC couplings) represent functionally distinct circuit dynamics that are temporally and behaviorally interspersed among theta-dominated modes during navigation. As such, delta modes could play a fundamental role in coordinating encoding and retrieval mechanisms or decision-making processes at a timescale that segments event sequences within behavioral episodes. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

SUBMITTER: Schultheiss NW

PROVIDER: S-EPMC8193833 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Contrary to cats and primates, cortical contribution to hindlimb locomotor movements is not critical in rats. However, the importance of the motor cortex to regain locomotion after neurological disorders in rats suggests that cortical engagement in hindlimb motor control may depend on the behavioral context. To investigate this possibility, we recorded whole-body kinematics, muscle synergies, and hindlimb motor cortex modulation in freely moving rats performing a range of natural locomotor procedures. We found that the activation of hindlimb motor cortex preceded gait initiation. During overground locomotion, the motor cortex exhibited consistent neuronal population responses that were synchronized with the spatiotemporal activation of hindlimb motoneurons. Behaviors requiring enhanced muscle activity or skilled paw placement correlated with substantial adjustment in neuronal population responses. In contrast, all rats exhibited a reduction of cortical activity during more automated behavior, such as stepping on a treadmill. Despite the facultative role of the motor cortex in the production of locomotion in rats, these results show that the encoding of hindlimb features in motor cortex dynamics is comparable in rats and cats. However, the extent of motor cortex modulations appears linked to the degree of volitional engagement and complexity of the task, reemphasizing the importance of goal-directed behaviors for motor control studies, rehabilitation, and neuroprosthetics. SIGNIFICANCE STATEMENT:We mapped the neuronal population responses in the hindlimb motor cortex to hindlimb kinematics and hindlimb muscle synergies across a spectrum of natural locomotion behaviors. Robust task-specific neuronal population responses revealed that the rat motor cortex displays similar modulation as other mammals during locomotion. However, the reduced motor cortex activity during more automated behaviors suggests a relationship between the degree of engagement and task complexity. This relationship emphasizes the importance of the behavioral procedure to engage the motor cortex during motor control studies, gait rehabilitation, and locomotor neuroprosthetic developments in rats.

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Awake delta and theta-rhythmic hippocampal network modes during intermittent locomotor behaviors in the rat.

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