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Whishaw, I. Q.

Publications and source records attributed to Whishaw, I. Q..

16 recordsLinked to original sources

Movements for Grooming in Rhesus Macaques Co-opted from Feeding Movements

Abstract Catarrhine primates exhibit a wide range of skilled hand movements, including those used for foraging and grooming, and their evolution attracts ongoing attention. Competing hypotheses are that skilled hand movements evolved for feeding, or that the hand movements of various behaviors evolved independently. The present study addressed these questions by asking whether the movements of grooming of rhesus macaques (Macaca mulatta) are co-opted from feeding movements. We video-recorded free-ranging rhesus macaques in the Cayo Santiago colony of the Caribbean Primate Research Center (CPRC), University of Puerto Rico. Allogrooming (grooming a conspecific), self-grooming, and rhythmic scratching with a hand or foot were compared with a common foraging behavior, geophagy, mining and eating soil. Allogrooming, self-grooming, and foraging occurred in visually mediated bouts that featured numerous comb and brush hand movements directed toward searching for a target in the fur or soil. Once located, the target was grasped between the thumb and index finger in a pincer grip to be placed in the mouth - or less often bitted or licked from the fur. Hand movements were generally directed toward the actor but were also influenced by object-surface features, including fur direction during grooming and the rocks and debris covering soil targets during geophagy. The grooming movements of comb, brush, and grasp were recognizably those used during foraging. Rhythmic scratching with a hand or foot was not visually guided but did employ a comb movement of the digits of the hand or foot. Thus, with the exception of the rhythmicity of scratching, the hand movements of grooming are fundamentally foraging movements. It is proposed that grooming movements are coopted from oromanual feeding movements in macaques, a relationship that may be widespread in other species.

animal behavior and cognition↗

Refinement and Retrospective Shift of the CA1 Place Code during Food-Carrying Decisions

Food carrying is an adaptive component of foraging that integrates resource evaluation with home-directed navigation, providing a naturalistic model for investigating how the brain organizes goal-directed behaviour. Despite extensive work on hippocampal coding during navigation and homing, how CA1 representations are reorganized when animals spontaneously transport acquired food home remains largely unexplored. We recorded dorsal CA1 population activity using one-photon calcium imaging with a V4 Miniscope while mice performed a self-paced foraging task in which food could be consumed at the acquisition site followed by a homeward return or carried to the home for consumption. Mice preferentially carried larger pellets, indicating that transport behaviour was sensitive to resource value. CA1 spatial coding differed systematically across behavioural outcomes. During carry-homeward runs, spatial representations were sparser, conveyed more spatial information, and showed greater trial-to-trial stability than during eat-inward runs, indicating a more precise and reliable place code during home-directed transport. Place fields also shifted forward during carrying, consistent with a retrospective bias toward recently traversed locations. By linking a self-generated food-handling decision to coordinated changes in the precision, stability, and temporal organization of CA1 activity, these findings extend hippocampal spatial-coding frameworks from trained navigation to ecologically grounded foraging behaviour.

neuroscience↗

Ecological Suboptimality in Naturalistic Foraging: Amplified Deviation from Optimality in a Mouse Model of Alzheimer Disease

Adaptive decision-making extends beyond selecting among discrete alternatives. It requires the dynamic organization of actions as costs, opportunities, and goals evolve over time. Foraging captures this complexity in an evolutionarily conserved behavior that integrates spatial, temporal, and reward-related information across successive actions. These demands make foraging an ecologically grounded framework for investigating Alzheimer disease, in which spatial cognition, temporal organization, cost evaluation, and behavioral flexibility are frequently disrupted. We examined foraging-related action selection in control C57BL/6J mice and APPNL-G-F knock-in mice using a controlled task in which travel distance, food texture, and pellet size altered the costs and benefits of available strategies. Bayesian multinomial modeling showed that control mice flexibly redistributed their behavior across conditions, whereas APPNL-G-F mice showed impaired cost integration, increased withdrawal, and reduced behavioral flexibility rather than a generalized performance impairment. Comparison with a classical reward-rate-maximization benchmark revealed substantial suboptimality in both groups. Control mice achieved 53% of the predicted optimal reward rate, whereas APPNL-G-F mice achieved 45%. These systematic departures suggest that behavior was shaped by cognitive, motivational, or contextual constraints not represented in the normative model, with Alzheimer-disease-relevant dysfunction associated with greater suboptimality. Group differences were greatest when optimal behavior was highly sensitive to competing costs. By preserving the distribution of behavior across strategies, this study establishes foraging-related action selection as a sensitive framework for detecting disease-associated disruptions that may be obscured by conventional measures of choice or overall task performance.

neuroscience↗

DISTINCT NEURAL SIGNATURES OF HIPPOCAMPAL POPULATION DYNAMICS DURING LOCOMOTION-IN-PLACE

Hippocampal CA1 neurons modulate their activity with movement variables such as time, distance, and speed, yet it remains unclear how these representations reorganize across behavioral states, from externally driven to self-paced movement and immobility. Here, we investigated how sensory events that initiate or terminate locomotion, structure CA1 population codes and how these codes reorganize across sensory-driven locomotion, spontaneous locomotion, and forced immobility. Using two-photon calcium imaging in head-fixed Thy1-GCaMP mice (n = 5) performing the air-induced running task on a non-motorized conveyor belt, we examined neuronal firing-rate modulation across a series of behavioral configurations designed to probe distinct forms of locomotion-in-place. In the No-Brake (locomotion-permitted) condition, the belt rotated freely, allowing animals to execute full cyclic limb movements in response to air stimulation. In the Brake (immobility) condition, the belt was fixed, restricting movement to partial or attempted locomotor motions. Firing-rate modulation with respect to time, distance, and speed was quantified using linear (Pearson correlation) and nonlinear (mutual information) metrics under permutation testing in the natural reference domains. Behaviorally, air stimuli produced faster, sustained running during air-on and more variable, self-paced movement during air-off. Neurally, a larger fraction of CA1 cells was active and significantly modulated during air-off. Within the modulated set, singularly tuned cells (time, distance, or speed) predominated over mixed-tuned cells, and speed-modulated cells peaked earlier after stimulus onset or offset than time- or distance-modulated cells. Under Brake, CA1 activity was predominantly singularly tuned to time or movement-in-place, with stronger movement modulation and engagement post-stimulation. Despite substantial single-cell turnover across configurations and phases, population-level analyses revealed a coherent, air-phase-locked organization and distinct movement-related populations across Brake and No-Brake conditions. These results indicate a state-dependent reweighting of sensorimotor features implemented atop a conserved ensemble scaffold in CA1.

neuroscience↗

Specialized for the reach: Fruit picking and positional behavior favor a reach over a grasp phenotype for Geoffroy's spider monkey (Ateles geoffroyi )

The Geoffroys spider monkey (Ateles geoffroyi) has distinctive features, including a vestigial external thumb, long fingers and forelimbs, and a prehensile tail. To better understand how its derived morphology is used during natural foraging, we filmed wild spider monkeys well habituated to human observers in Sector Santa Rosa (SSR), Area de Conservacion Guanacaste in northwestern Costa Rica. We analyzed frame-by-frame video recordings to examine the influence of this morphology on picking 14 fruit species. The spider monkeys most frequent reach strategy was a branch-withdraw (62%: 1,338 of 2,164 fruit items), in which they reached equally with either hand for a branch, hooked their fingers around it, and pulled it toward themselves to take the attached fruit by mouth. Less frequently they picked fruit by hand (466 observations) or only by mouth (360 observations). Hand and arm extension, with rotatory movements at the wrist, elbow, and shoulder, assisted reaching and transferring food to the mouth, and tail prehension further assisted extending reaches horizontally and ventrally into the tree canopy. To pick fruit by hand, they used tactile guidance and finger pad-to-palm grasps, mainly with the second digit (index finger), and rotatory arm and head movements to deliver fruit from the hand to the mouth. Fruit was grasped by the incisors and chewed with molars to release the endocarp for swallowing, with the exocarp sometimes ejected by spitting. The combination of branch-withdrawal, mouth grasping and postural extension via a prehensile tail constitutes a "reach" phenotype that contrasts with the "grasp" phenotype of the sympatric capuchin monkey. The behavioral and morphological commitment to a reach phenotype in spider monkeys supports the idea that the reach and the grasp have separate evolutionary histories and, with respect to spider and capuchin monkeys, contribute to niche partitioning. "Spider monkeys cast a distinct morphological silhouette - long scrawny arms and a snaky prehensile tail arching from a narrow pot-belly torso, topped by a small round head and blunt face. The commitment of this relatively large-bodied platyrrhine to a large-tree, upper canopy milieu and to ripe fruit foraging is seen throughout its skeletal and craniodental morphology." Rosenbert et al (2008).

animal behavior and cognition↗

Gaze audits food items for bite points during human withdraw-to-eat movements

Food handling and eating are central to the skill of primate hand movements, and their analysis can provide insights into the evolutionary origins of hand use and its generalization to other behaviors, such as tool use. Vision contributes differently to the reach, grasp, and withdraw-to-eat components of hand use when eating, suggesting that these component movements are controlled by different visuomotor networks with distinct evolutionary histories. This study examines the role of gaze in mediating the withdraw-to-eat movement in human participants eating various food items, including candy, donuts, carrots, bananas, and apples, or pantomiming the eating movements for some of these items. Eye-tracking and frame-by-frame video analyses are used to describe gaze, gaze duration, gaze disengagement, eye blinking, and hand preference in eating each food item. The results show that gaze first identifies points on a food item that the dominant hand can grasp and then identifies points on the food item that the mouth can bite. The hand and finger shaping movements of both the initial grasp and subsequent food handling aid in exposing targets on the food for grasping and biting. The comparison of real and pantomime eating suggests that only real food items possess the affordances that elicit gaze patterns associated with identifying online targets for grasps and bites. The findings are discussed in relation to idea that gaze has a feature-detector-like role linking food cues to the skilled movements of hand shaping to grasp a food item and then to orient a food item to the mouth for biting.

animal behavior and cognition↗

Cortical network and projection neuron types that articulate serial order in a skilled motor behavior

The coordination of forelimb and orofacial movements to compose an ethological reach-to-consume behavior likely involves neural communication across brain regions. Leveraging wide-field imaging and photo-inhibition to survey across the cortex, we identified a cortical network and a high-order motor area (MOs-c), which coordinate action progression in a mouse reach-and-withdraw-to-drink (RWD) behavior. Electrophysiology and photo-inhibition across multiple projection neuron types within the MOs-c revealed differential contributions of pyramidal tract and corticothalamic (CTMOs) output channels to action progression and hand-mouth coordination. Notably, CTMOs display sustained firing throughout RWD sequence and selectively enhance RWD-relevant activity in postsynaptic thalamus neurons, which also contribute to action coordination. CTMOs receive converging monosynaptic inputs from forelimb and orofacial sensorimotor areas and are reciprocally connected to thalamic neurons, which project back to the cortical network. Therefore, motor cortex corticothalamic channel may selectively amplify the thalamic integration of cortical and subcortical sensorimotor streams to coordinate a skilled motor sequence.

neuroscience↗

The platyrrhine primate Cebus imitator uses gaze to adjust grasp posture for food handling and withdraw to the mouth

Orienting a food item held in the hand to withdraw it to the mouth for eating is mediated by vision in catarrhine anthropoids and by nonvisual strategies in strepsirrhines. The present study asks whether vision contributes to the withdraw in a platyrrhine anthropoid, a member of a monophyletic primate suborder whose stem group diverged from catarrhines about 40 million years ago. We examined gaze and hand use in arboreal fruit picking by the Costa Rican capuchin, Cebus imitator, a platyrrhine known for its skilled object-handling and tool use. Videos clips of reach, grasp and withdraw movements and associated gaze were examined frame-by-frame to assess hand shaping and sensory control of eating. Cebus imitator used vision and touch to reach for and grasp food items with precision or whole hand grasps. They used vision to orient food items held inhand into a precision grip and their withdraw of food items to the mouth was assisted with a vertically oriented hand. The conjoint use of vision, grasp and hand posture by capuchins is discussed in relation to the staged evolution of visual manipulation of objects, one of which is featured in this platyrrhine primate.

evolutionary biology↗

Generation of a hybrid AppNL-G-F/NL-G-F xThy1-GCaMP6s+/- Alzheimer disease mouse mitigates the behavioral and hippocampal encoding deficits of APP knock-in mutations of AppNL-G-F/NL-G-F mice

In contrast to most transgenic mouse models of Alzheimer disease (AD), knock-in mice expressing familial AD-linked mutations of the amyloid precursor protein (App) gene exhibit stereotypical age-dependent amyloid beta (A{beta}) pathology and cognitive impairment without physiologically unrealistic App overexpression. This study investigated the effect of familial AD-linked App mutations on hippocampal CA1 neuronal activity and function. To enable calcium imaging of neuronal activity, AppNL-G-F/NL-G-F knock-in (APPki) mice were crossed with Thy1-GCaMP6s+/- (C-TG) mice to generate AppNL-G-F/NL-G-FxThy1-GCaMP6s+/- (A-TG) mice, which were characterized at 12 months of age. A-TG mice exhibited A{beta} pathology in the hippocampus. In several configurations of an air-induced running task, A-TG mice and C-TG mice were equally successful in learning to run or to stay immobile. In the Morris water place test, A-TG mice were impaired, but learned the task. Comparisons of hippocampal CA1 neuronal activity in the air-induced running task showed that A-TG mice displayed neuronal hypoactivity both during movement and immobility. A-TG mice and C-TG CA1 neuronal encoding of distance or time in the air induced running task were not different. These results suggest that knock-in of familial AD-linked mutations in A-TG mice results in A{beta} pathology, neuronal hypoactivity, and cognitive impairment without severely affecting CA1 neuronal encoding. In comparison to APPki mice, A-TG mice had less severe AD-like memory impairments at 12 months of age (Saito et al., 2014; Mehla et al., 2019), suggesting that the disease onset was delayed in A-TG mice. The effect of APP mutations may have been mitigated through genetic mechanisms when APPKi mice were crossed with C-TG mice.

neuroscience↗

Conjunctive and complementary CA1 hippocampal cell populations relate sensory events to immobility and locomotion

This study investigated the dynamics of recruitment of cells in the CA1 region of the hippocampus in response to sensory stimuli presented during immobility, movement, and their transitions. Two-photon calcium imaging of somal activity in CA1 neuron populations was done in head fixed mice. Sensory stimuli, either a light flash or an air stream, were delivered to the mice when at rest, when moving spontaneously, and while they were induced to run a fixed distance on the conveyor belt. Overall, 99% of 2083 identified cells (from 5 mice) were active across one or more of 20 sensorimotor events. A larger proportion of cells were active during locomotion. Nevertheless, for any given sensorimotor event, only about 17% of cells were active. When considering pairs of sensorimotor event types, the active cell population consisted of conjunctive (C [isin] A and B) cells, active across both events, and complementary (C [isin] A not B or C [isin] B not A) cells that were active only during individual events. Whereas conjunctive cells characterised stable representations of repeated sensorimotor events, complementary cells characterised recruitment of new cells for encoding novel sensorimotor events. The moment-to-moment recruitment of conjunctive and complementary cells across changing sensorimotor events signifies the involvement of the hippocampus in functional networks integrating sensory information with ongoing movement. This role of the hippocampus is well suited for movement guidance that secondarily might include spatial behavior, episodic learning and memory, context representation, and scene construction.

neuroscience↗

String-Pulling as a Behavioral Assessment of Skilled Forelimb Motor Function in a Middle Cerebral Artery Occlusion Rat Model

Stroke is a leading cause of long-term disability in humans and frequently results in bilateral impairments in fine motor control. Many behavioral tasks used to assess rodent models of stroke evaluate a single limb; however, recent work has demonstrated that bilateral hand-over-hand movements used to pull in a string assess skilled movement of both hands. Devascularization focused on the forelimb portion of sensorimotor cortex has been observed to produce persistent disruptions in the topographical organization of string-pulling behavior. The current study examined changes in string-pulling after a more clinically relevant rodent model of stroke via middle cerebral artery occlusion (MCAO). Detailed movement analyses revealed disruptions in the bilateral organization of string-pulling and fine motor control of both hands. Rats missed the string more often with both hands, and when the string was missed on the impaired side, rats continued to cycle through subcomponents of string-pulling behavior as if the string were grasped in the hand. Rats also failed to make a grasping motion with the impaired hand when the string was missed and instead, demonstrated an open-handed raking-like motion. No differences were found in time to approach or to complete the string-pulling task to obtain a reward, demonstrating the importance of using a detailed functional analysis of movement to detect changes in performance. String-pulling behavior is sensitive at detecting changes in bilateral rhythmical hand control following MCAO providing a foundation for future work to investigate other models of stroke and to evaluate the efficacy of therapeutic interventions that enhance neuroplasticity.

animal behavior and cognition↗

Two types of hand withdraw movement to place food in the mouth mediated by somatosensation in 22-species of strepsirrhines

The evolution of visual control of the hand to assist feeding by primates is uncertain but in anthropoid primates vision contributes not only to reaching for food and grasping it but also to the withdraw movement that brings food to the mouth. The strepsirrhines are a relatively large monophyletic group of Euarchontoglires near the base of the primate cladogram that are described as using vision to reach for food, but it is not known whether they use vision to assist the withdraw movement. The present study answere this question in 22 species of captive strepsirrhines from 6 of the seven strepsirrhine families, Daubentoniidae, Cheirogaleidae, Indriidae, Lemuridae, Lorisidae and Galagidae. Animals were videorecorded as they ate their normal food provisions. Dependent measures for analyses were ground withdraw movements, bringing grasped food to the mouth, and inhand withdraw movements, brining food held in the hand to the mouth, as well as the posture and head movements associated with each type of withdraw. Frame-by-frame scores from the video record showed that there were large differences between and within strepsirrhine families in these movements. Nevertheless, for all species, the withdraw movement was mediated by somatosensation, with mouth reaching and perioral contact with food determining how food was eventually eaten. Nonvisual behavior also contributed to food grasping as many species sniffed food before or during grasping. Even amongst species that made most use of the hand for their withdraws, the insectivores Loris lydekkerianus and Galago senegalensis, and herbivores, Hapalemur simus and Eulemur flavifrons, perioral contact was used to orient food for biting. The use of somatosensation and the absence of vision in mediating getting food in strepsirrhines suggests that visual mediation of the withdraw is an anthropoid innovation.

animal behavior and cognition↗

Data-driven analysis of rat pup behavior reveals novel effects of maternal pre-conception exposure to nicotine

We present a deep neural network for data-driven analyses of infant rat behavior in an open field task. The network was applied to study the effect of maternal nicotine exposure prior to conception on offspring motor development. The neural network outperformed human expert designed animal locomotion measures in distinguishing rat pups born to nicotine exposed dams versus control dams. Notably, the network discovered novel movement alterations in posture, movement initiation and a stereotypy in "warm-up" behavior (the initiation of movement along specific dimensions) that were predictive of nicotine exposure. The results suggest that maternal preconception nicotine exposure delays and alters offspring motor development. In summary, we demonstrated that a deep neural network can automatically assess animal behavior with high accuracy, and that it offers a data-driven approach to investigating pharmacological effects on brain development. SignificanceRelating neuronal activity to behavior is crucial to understand brain function. Despite the staggering progress in monitoring brain activity, behavioral analyses still do not differ much from methods developed 30-50 years ago. The reason for that is the difficulty for automated video analyses to detect small differences in complex movements. Here we show that applying deep neuronal networks for automated video analyses can help to solve this problem. More importantly, knowledge extracted from the network allowed to identify subtle changes in multiple behavioral components, which were caused by maternal preconception nicotine exposure in rat pups. Thus, the examples presented here show how neuronal networks can guide the development of more accurate behavioral tests to assess symptoms of neurological disorders.

neuroscience↗

A toolbox for automated video analysis of rodents engaged in string-pulling: Phenotyping motor behavior of mice for sensory, whole-body and bimanual skilled hand function

String-pulling in rodents (rats and mice) is a task in which animals make hand-over-hand movements to spontaneously reel in a string with or without a food reward attached to its end. The task elicits bilateral skilled hand movements for which rodents require little training. The task is suitable for phenotyping physiology and pathophysiology of sensorimotor integration in rodent models of neurological and motor disorders. Because a rodent stands in the same location and its movements are repetitive, the task lends itself to quantification of topographical and kinematic parameters for on-line tactile tracking of the string, skilled hand movements for grasping, and rhythmical bilateral forearm movements to advance the string. Here we describe a Matlab(R) based software with a graphical user interface to assist researchers in analyzing the video record of string pulling. The software allows global characterization of position and motion using optical flow estimation, descriptive statistics, principal component, and independent component analyses as well as temporal measures of Fano factor, entropy, and Higuchi fractal dimension. Based on image segmentation and object tracking heuristic algorithms, the software also allows independent tracking of the body, ears, nose, and forehands for estimation of kinematic parameters such as body length, body angle, head roll, head yaw, head pitch, movement paths and speed of hand movement. The utility of the task and that of the software is presented by describing mouse strain characteristics in string-pulling behavior of two strains of mice, C57BL/6 and Swiss Webster. Postural and skilled hand kinematic differences that characterize the strains highlight the utility of the task and assessment methods for phenotypic and neurological analysis of healthy and rodent models of diseases such as Parkinsons, Huntingtons, Alzheimers and other neurological and motor disorders. Significance statementMouse models are used to investigate the physiology and pathophysiology of motor deficits observed in human neurological conditions, for testing substances for therapeutic drug development, and to investigate the role of neural systems and their genetic basis in the expression of behavior. Behavioral tasks involving unconditioned and natural behavior can provide rich insights into motor performance in animal models and analyses can be aided by the automated processing of video data for reliable quantification and high throughput.

neuroscience↗

Reach and Grasp Altered in Pantomime String-Pulling: A Test of the Action/Perception Theory in a Bilateral Reaching Task

The action/perception theory of cortical organization is supported by the finding that pantomime hand movements of reaching and grasping are different from real movements. Frame-by-frame video analysis and MATLAB(R) based tracking examined real/pantomime differences in a bilaterally movement, string-pulling, pulling down a rope with hand-over-hand movements. Sensory control of string-pulling varied from visually-direct when cued, visually-indirect when non cued and somatosensory controlled in the absence of vision. Cued grasping points were visual tracked and the pupils dilated in anticipation of the grasp, but when noncued, visual tracking and pupil responses were absent. In real string-pulling, grasping and releasing the string featured an arpeggio movement in which the fingers close and open in the sequence 5 through 1 (pinki first, thumb last); in pantomime, finger order was reversed, 1 through 5. In real string-pulling, the hand is fully opened and closed to grasp and release; in pantomime, hand opening was attenuated and featured a gradual opening centered on the grasp. The temporal structure of arm movements in real string-pulling featured up-arm movements that were faster than down-arm movement. In pantomime, up/down movements had similar speed. In real string-pulling, up/down arm movements were direct and symmetric; in pantomime, they were more circular and asymmetric. That pantomime string-pulling featured less motoric and temporal complexity than real string-pulling is discussed in relation to the action/perception theory and in relation to the idea that pantomimed string-pulling may feature the substitution of gestures for real movement.\n\nSignificant StatementMost laboratory studies investigating hand movements made by humans feature single hand movements, the current study presents a novel string-pulling task to study bimanual coordination of left and right hands in real and pantomime conditions. The results show that pantomime string-pulling featured less motoric and temporal complexity than real string-pulling. These findings are relevant to the contemporary theory of action and perception that the dorsal stream (parietal cortex) is related to actions and the ventral stream (temporal cortex) is related to perception.

neuroscience↗

Low acetylcholine during early sleep is important for motor memory consolidation

The synaptic homeostasis theory of sleep proposes that low neurotransmitter activity in sleep is optimal for memory consolidation. We tested this theory by asking whether increasing acetylcholine levels during early sleep would disrupt motor memory consolidation. We trained separate groups of adult mice on the rotarod walking and skilled reaching for food tasks, and after training, administered physostigmine, an acetylcholinesterase inhibitor, to increase cholinergic tone in subsequent sleep. Post-sleep testing suggested that physostigmine impaired motor skill acquisition. Home-cage video monitoring and electrophysiology revealed that physostigmine disrupted sleep structure, delayed non-rapid-eye-movement sleep onset, and reduced slow-wave power in the hippocampus and cortex. The impaired motor performance with physostigmine, however, was not solely due to its effects on sleep structure, as one hour of sleep deprivation after training did not impair rotarod performance. A reduction in cholinergic tone by inactivation of cholinergic neurons during early sleep also affected rotarod performance. Administration of agonists and antagonists of muscarinic and nicotinic acetylcholine receptors revealed that activation of muscarinic receptors during early sleep impaired rotarod performance. The experiments suggest that the increased slow wave activity and inactivation of muscarinic receptors during early sleep due to reduced acetylcholine contribute to motor memory consolidation.

neuroscience↗