Skilled reaching in rats and humans: evidence for parallel development or homology

doi:10.1016/S0166-4328(05)80252-9

Behavioural Brain Research

Volume 47, Issue 1, 15 March 1992, Pages 59-70

https://doi.org/10.1016/S0166-4328(05)80252-9 Get rights and content

Forelimb reaching by the rat is used as a paradigm for the experimental study of neural control, plasticity, and recovery of function after injury, in the expectation that results are generalizable to humans. The present study was done to compare rat, to human reaching movements. The movements of both species were videorecorded and subjected to frame-by-frame analysis using Cartesian (spatial and velocity) and Eshkol-Wachman Movement Notation (EWMN) systems. The component movements of reaching, their sequence and velocity profiles, and their topography were similar in the two species. Both species also displayed more supination and lengthened grasping times when reaching for small as opposed to large objects. Both rats and humans moved the limb medially using the upper, arm to aim it when they were required to reach through an aperture but in a free reaching test only rats continued to aim the limb. Human movements were characterized by greater blending of movement components, more variability, and independent digit use. Arguments are presented that the similarities and differences in rat and human reaching are not trivially accounted for by limb and task similarities. The many similarities in the movements of the two species provide evidence for at least parallel development or perhaps even homology.

References (50)

AtzJ.W.
The application of the idea of homology to behavior
BishopA
Use of the hand in lower primates
BurešJ. et al.
The control of movements by the motor cortex
BráchaV. et al.
The reaching reaction in the rat: a part of the digging pattern?
Behav. Brain Res.
(1990)
BucyP.C. et al.
Destruction of the ‘pyramidal tract’ in man
J. Neurosurg.
(1964)
CastroA.J.
The effects of cortical ablations on digital usage in the rat
Brain Res.
(1972)
CastroA.J.
Motor performance in rats, the effects of pyramidal tract section
Brain Res.
(1972)
DonoghueJ.P. et al.
The motor cortex of the rat: cytoarchitecture and microstimulation mapping
J. Comp. Neurol.
(1982)
DunnettS.B. et al.
Striatal grafts in rats with unilateral lesions. III. Recovery from dopamine-dependent motor asymmetry and deficits in skilled paw reaching
Neuroscience
(1988)
DunnettS.B. et al.
Dopamine-rich grafts ameliorate whole body motor asymmetry and sensory neglect but not independent skilled limb use in rats with 6-hydroxydopamine lesions
Brain Res.
(1987)

EshkolN. et al.

FrommC. et al.

Relation of motor cortex neurons to precisely controlled and ballistic movements

Neurosci. Lett.

(1977)

GanorI. et al.

Coordination and integration in the hindleg step cycle of the rat: kinematic synergies

Brain Res.

(1980)

GeorgopoulosA.P. et al.

On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex

J. Neurosci.

(1982)

GolaniI.

Homeostatic motor processes in mammalian interactions: A choreography of display

GolaniI. et al.

A proposed natural geometry of recovery from akinesia in the lateral hypothalamic rat

Brain Res.

(1979)

HodosW.

The concept of homology and the evolution of behavior

JeannerodM.

JollyA

Prosimians' manipulation of simple object problems

Anim. Behav.

(1964)

KennardM.A.

Cortical reorganization of motor function: studies on a series of monkeys of various ages from infancy to maturity

Arch. Neurol. Psychiatry

(1942)

KuypersH.G.J.M.

Anatomy of the descending pathways

KwanH.C. et al.

Spatial organization of precentral cortex in awake primates. II. Motor outputs

J. Neurophysiol.

(1978)

LarsonC.F. et al.

Hand preference and whole-body turning biases of lesser bushbabies (Galago senegalensis)

Brain Gehav. Evol.

(1989)

LassekA.M.

LawrenceD.G. et al.

The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions

Brain

(1968)

Cited by (154)

Impairments and compensation in string-pulling after middle cerebral artery occlusion in the rat
2023, Behavioural Brain Research
Stroke is a leading cause of long-term disability in humans, and it is frequently associated with impairments in the skilled use of the arms and hands. Many human upper limb impairments and compensatory changes have been successfully modeled in rodent studies of neocortical stroke, especially those that evaluate single limb use in tasks, such as reaching for food. Humans also use their hands for bilaterally coordinated movements, dependent upon interhemispheric cortical projections, which are also compromised by unilateral stroke. This study describes middle cerebral artery occlusion (MCAO) dependent changes in the bilaterally dependent hand use behavior of string-pulling in the rat. The task involves making hand-over-hand movements to pull down a string that contains a food reward attached to its end. MCAO rats missed the string more often with both hands than Sham rats. When the string was missed on the contralateral to MCAO body 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 contralateral to MCAO hand when the string was missed and instead, demonstrated an open-handed raking-like motions. Nevertheless, with repeated attempts, rats performed components of string-pulling well enough to obtain a reward on the end of the string. Thus, string-pulling behavior is sensitive to bilateral impairments but is achieved with compensatory adjustments following MCAO. These aspects of MCAO string-pulling provide a foundation for studies that investigate the efficacy of therapeutic intervention which might enhance neuroplasticity and recovery.
AutoRG: An automatized reach-to-grasp platform technology for assessing forelimb motor function, neural circuit activation, and cognition in rodents
2023, Journal of Neuroscience Methods
Rodent reach-to-grasp function assessment is a translationally powerful model for evaluating neurological function impairments and recovery responses. Existing assessment platforms are experimenter-dependent, costly, or low-throughput with limited output measures. Further, a direct histologic comparison of neural activation has never been conducted between any novel, automated platform and the well-established single pellet skilled reach task (SRT).
To address these technological and knowledge gaps, we designed an open-source, low-cost Automatized Reach-to-Grasp (AutoRG) pull platform that reduces experimenter interventions and variability. We assessed reach-to-grasp function in rats across seven progressively difficult stages using AutoRG. We mapped AutoRG and SRT-activated motor circuitries in the rat brain using volumetric imaging of the immediate early gene-encoded Arc (activity-regulated cytoskeleton-associated) protein.
Rats demonstrated robust forelimb reaching and pulling behavior after training in AutoRG. Reliable force versus time responses were recorded for individual reach events in real time, which were used to derive several secondary functional measures of performance. Moreover, we provide the first demonstration that for a training period of 30 min, AutoRG and SRT both engage similar neural responses in the caudal forelimb area (CFA), rostral forelimb area (RFA), and sensorimotor area (S1).
AutoRG is the first low-cost, open-source pull system designed for the scale-up of volitional forelimb motor function testing and characterization of rodent reaching behavior. The similarities in neuronal activation patterns observed in the rat motor cortex after SRT and AutoRG assessments validate the AutoRG as a rigorously characterized, scalable alternative to the conventional SRT and expensive commercial systems.
Reaching an understanding of cortico-medullary control of forelimb behaviors
2023, Cell
Patterned Stimulation of the Chrimson Opsin in Glutamatergic Motor Thalamus Neurons Improves Forelimb Akinesia in Parkinsonian Rats
2022, Neuroscience
Parkinson’s disease (PD) is a motor disorder charactertised by altered neural activity throughout the basal ganglia-thalamocortical circuit. Electrical deep brain stimulation (DBS) is efficacious in alleviating motor symptoms, but has several notable side-effects, most likely reflecting the non-specific nature of electrical stimulation and/or the brain regions targeted. We determined whether specific optogenetic activation of glutamatergic motor thalamus (Mthal) neurons alleviated forelimb akinesia in a chronic rat model of PD. Parkinsonian rats (unilateral 6-hydroxydopamine injection) were injected with an adeno-associated viral vector (AAV5-CaMKII-Chrimson-GFP) to transduce glutamatergic Mthal neurons with the red-shifted Chrimson opsin. Optogenetic stimulation with orange light at 15 Hz tonic and a physiological pattern, previously recorded from a Mthal neuron in a control rat, significantly increased forelimb use in the reaching test (p < 0.01). Orange light theta burst stimulation, 15 Hz and control reaching patterns significantly reduced akinesia (p < 0.0001) assessed by the step test. In contrast, forelimb use in the cylinder test was unaffected by orange light stimulation with any pattern. Blue light (control) stimulation failed to alter behaviours. Activation of Chrimson using complex patterns in the Mthal may be an alternative treatment to recover movement in PD. These vector and opsin changes are important steps towards translating optogenetic stimulation to humans.
Modulation of neural co-firing to enhance network transmission and improve motor function after stroke
2022, Neuron
Stroke is a leading cause of disability. While neurotechnology has shown promise for improving upper limb recovery after stroke, efficacy in clinical trials has been variable. Our central thesis is that to improve clinical translation, we need to develop a common neurophysiological framework for understanding how neurotechnology alters network activity. Our perspective discusses principles for how motor networks, both healthy and those recovering from stroke, subserve reach-to-grasp movements. We focus on neural processing at the resolution of single movements, the timescale at which neurotechnologies are applied, and discuss how this activity might drive long-term plasticity. We propose that future studies should focus on cross-area communication and bridging our understanding of timescales ranging from single trials within a session to across multiple sessions. We hope that this perspective establishes a combined path forward for preclinical and clinical research with the goal of more robust clinical translation of neurotechnology.
Oscillatory waveform sharpness asymmetry changes in motor thalamus and motor cortex in a rat model of Parkinson's disease
2022, Experimental Neurology
Parkinson's disease (PD) causes bursty and oscillatory activity in basal ganglia output that is thought to contribute to movement deficits through impact on motor thalamus and motor cortex (MCx). We examined the effect of dopamine loss on motor thalamus and motor cortex activity by recording neuronal and LFP activities in ventroanterior-ventrolateral (VAVL) thalamus and MCx in urethane-anesthetised control and parkinsonian rats. Dopamine lesion decreased the firing rate and increased the bursting of putative pyramidal neurons in layer V, but not layer VI, of the MCx without changing other aspects of firing pattern. In contrast, dopamine lesion did not affect VAVL firing rate, pattern or low threshold calcium spike bursts. Slow-wave (~1 Hz) oscillations in LFP recordings were analyzed with conventional power and waveform shape analyses. While dopamine lesion did not influence total power, it was consistently associated with an increase in oscillatory waveform sharpness asymmetry (i.e., sharper troughs vs. peaks) in both motor thalamus and MCx. Furthermore, we found that measures of sharpness asymmetry were positively correlated in paired motor thalamus-MCx recordings, and that correlation coefficients were larger in dopamine lesioned rats. These data support the idea that dysfunctional MCx activity in parkinsonism emerges from subsets of cell groups (e.g. layer V pyramidal neurons) and is evident in the shape but not absolute power of slow-wave oscillations. Hypoactive layer V pyramidal neuron firing in dopamine lesioned rats is unlikely to be driven by VAVL thalamus and may, therefore, reflect the loss of mesocortical dopaminergic afferents and/or changes in intrinsic excitability.

View all citing articles on Scopus

View full text

Skilled reaching in rats and humans: evidence for parallel development or homology

The application of the idea of homology to behavior

Use of the hand in lower primates

The control of movements by the motor cortex

The reaching reaction in the rat: a part of the digging pattern?

Behav. Brain Res.

Destruction of the ‘pyramidal tract’ in man

J. Neurosurg.

The effects of cortical ablations on digital usage in the rat

Brain Res.

Motor performance in rats, the effects of pyramidal tract section

Brain Res.

The motor cortex of the rat: cytoarchitecture and microstimulation mapping

J. Comp. Neurol.

Striatal grafts in rats with unilateral lesions. III. Recovery from dopamine-dependent motor asymmetry and deficits in skilled paw reaching

Neuroscience

Dopamine-rich grafts ameliorate whole body motor asymmetry and sensory neglect but not independent skilled limb use in rats with 6-hydroxydopamine lesions

Brain Res.

Relation of motor cortex neurons to precisely controlled and ballistic movements

Neurosci. Lett.

Coordination and integration in the hindleg step cycle of the rat: kinematic synergies

Brain Res.

On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex

J. Neurosci.

Homeostatic motor processes in mammalian interactions: A choreography of display

A proposed natural geometry of recovery from akinesia in the lateral hypothalamic rat

Brain Res.

The concept of homology and the evolution of behavior

Prosimians' manipulation of simple object problems

Anim. Behav.

Cortical reorganization of motor function: studies on a series of monkeys of various ages from infancy to maturity

Arch. Neurol. Psychiatry

Anatomy of the descending pathways

Spatial organization of precentral cortex in awake primates. II. Motor outputs

J. Neurophysiol.

Hand preference and whole-body turning biases of lesser bushbabies (Galago senegalensis)

Brain Gehav. Evol.

The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions

Brain