Ian Darian-Smith

Tactile discrimination of gratings

SummaryHuman subjects were required to differentiate grating surfaces of alternating grooves and ridges by moving a finger back and forth across the surface. Their discriminative capacities were measured, as well as the movement and force profiles that they selected. To measure discrimination, a forced choice paradigm was used in which three surfaces were presented on each trial. Two surfaces were the same (standards) and the subject was required to indicate which of the three surfaces (the comparison) differed from the other two. Two series of surfaces were used with standards whose spatial periods were 770 and 1002 μ, respectively. Subjects were able to discriminate, at the 75% correct level, two gratings which differed in spatial period by the order of 5%. When tangential movement between the surface and the finger was eliminated, and only radial contact permitted, discrimination was degraded and the 75% correct levels increased to the order of 10%. Subjects were free to choose their own patterns of finger movement and of contact force between finger and surface. Movement was measured cinematographically. For all subjects movement patterns were close to sinusoidal, with frequencies in the range of 4.0 Hz and with mean velocities of the order of 160 mm/s. Patterns of contact force were measured by a force transducer. For all subjects the force varied rhythmically in synchrony with movement, but the patterns and magnitudes varied with the subject. Gratings were scaled for perceived roughness by a magnitude estimation technique: the relationship between perceived roughness and grating period was monotonic.

Tactile discrimination of thickness.

SummaryThe ability of human subjects to discriminate plane metal plates of different thickness was measured using a forced-choice paradigm. The plates, made by electroplating a thin layer of copper onto flat brass shims, were gripped between the thumb and the index finger. Subjects were presented with either 2 standard plates (0.2 mm thick), or a standard plate and a test plate that was slightly thicker, and were required to state which alternative had occurred. When the edges of the plates could not be touched, a difference in thickness of about 0.075 mm could be discriminated. Surprisingly, when the edges were included in the grip, performance did not improve. All hypotheses of strategies used by the subjects required them to sense the angles of the finger joints with a precision of about 0.1°.

Corticospinal projection patterns following unilateral section of the cervical spinal cord in the newborn and juvenile macaque monkey

Immediately following a unilateral section of the midcervical spinal cord that interrupts the dorsolateral, lateral, and ventral columns, the macaque monkey has a severe flaccid paralysis on the side of the lesion. Recovery of hand function is rapid, and, although it is incomplete, within a few months, the monkey uses the initially disabled hand and fingers with considerable skill. We examined the accompanying changes in the pattern of projection of corticospinal neurons to the cervical spinal cord that occurred following such a lesion. Spinal section was done both in newborn and juvenile macaques, and the postlesion period was followed for up to 150 weeks. Corticospinal neuron populations were visualized by using both anterogradely and retrogradely transported labels, and their origins, spinal pathways, and terminations were examined at intervals during the period of recovery of hand function. Immediately following unilateral section of the spinal cord at C3, sampled counts of soma profiles of retrogradely labeled neurons indicated that there was a profound reduction in the corticospinal projection to the hemicord caudal to the lesion. The few labeled corticospinal axons spared by the lesion bypassed the spinal lesion by descending in the contralateral cord and then crossing the midline caudal to the lesion. A few corticospinal axons may also have bypassed the lesion in the ipsilateral ventromedial column when this was not fully interrupted by the lesion. In every monkey, we observed a similar, profound reduction in the corticospinal (and rubrospinal) projections to the hemicord caudal to the lesion: This pattern did not alter significantly over an extended recovery period. An unchanging corticospinal projection to the cervical spinal cord contralateral to the lesion was also visualized in each monkey and resembled that seen in the normal macaque. Although the resolution of the labeling and counting procedures used precluded the identification of small increases in the numbers of corticospinal neurons projecting to the hemicord caudal to the lesion, we concluded that there was no substantial reconstruction of this projection over a recovery period of more than 2 years. J. Comp. Neurol. 381:282‐306, 1997.

Manual dexterity and corticospinal connectivity following unilateral section of the cervical spinal cord in the macaque monkey

The macaque recovers quite rapidly from the immediate severe flaccid hemiparesis that results from unilateral section of the cervical spinal cord (between C3 and C6) and starts to use the impaired hand to pick up objects within about 30 days following the surgery. Within another 60 days, the monkey is quite dexterous; nonetheless, there is a persisting deficit. We used video recording to study the long‐term recovery of manual dexterity following unilateral section of the cervical cord in newborn and juvenile monkeys. A reach‐and‐retrieve manual task was examined. By using a preset oppositional force, opposition of the pads of the index finger and thumb in the vertical plane was needed to retrieve the desired target object. The corticospinal connectivity of each monkey was also examined by using retrograde or anterograde tracers at the end of the experimental period (Galea and Darian‐Smith [1997] J. Comp. Neurol., this issue) and was correlated with the manual performance.

Parallel pathways mediating manual dexterity in the macaque

Abstract Transmission of information along appropriately structured parallel pathways ensures that a great deal of information can be transferred from the source to the target very quickly, and with great security-essential features of any motor control system. Studies over the last two decades have established that the corticospinal and corticocerebellar pathways mediating manual dexterity in the primate are structurally organized to sustain the parallel transmission of sensorimotor information in multiple pathways. Serial, hierarchical control systems now seem insufficient to regulate voluntary hand movements. To achieve the required coordination, and precision and speed of execution, they must be combined with parallel control systems, which themselves incorporate elaborate feedforward and feedback controls. To illustrate these issues, two aspects of the structural organization of parallel sensorimotor pathways mediating manual dexterity in the macaque are reviewed. First, we examine the structure of the multiple corticospinal neuron subpopulations projecting from different areas of the frontoparietal cortex and how they are modified following hemisection of the cervical spinal cord. The remarkable recovery of hand function following spinal hemisection, despite the absence of any structural ’bridging’ of the interrupted spinal pathways, and the fact that this is accountable in a parallel but not in a purely serial transmission system, are then reviewed. The second aspect of parallel distributed transmission examined is its occurrence within a single population of relay neurons. Our recent structural analysis of the somatic/dendritic organization of rubrospinal neurons in macaque red nucleus is used. The very large dendritic fields of individual neurons, extending over one-third or more of the nucleus, provide a framework for extracting precise somatotopic information from an input population whose axon terminal arbors overlap extensively, and, which, without effective filtering, would provide poor spatial resolution.

MANUAL DEXTERITY: HOW DOES THE CEREBRAL CORTEX CONTRIBUTE?

1. Manual dexterity, of great evolutionary significance to the primates, ranges in complexity from the precise opposition of finger and thumb to Brendal playing Mozart. All dexterity depends on a sustained and rapid transfer of sensorimotor information between the cerebral cortex and the cervical spinal cord.

Skin profiles during sinusoidal vibration of the fingerpad

SummarySkin on the fingertips of humans and monkeys was stimulated by a probe vibrating with a sinusoidal displacement. The probe and the skin were illuminated stroboscopically and were viewed through a dissecting microscope. The stroboscope was triggered by the sinusoidal generator via a digital delay, so that the position of both the probe and the skin could be measured at regular intervals during the cycle. Six frequencies and 3 amplitudes of vibration were used. During a portion of the cycle the probe and the skin separated, so that the skin waveform was a clipped sinusoid. An increase in stimulus frequency increased the fraction of the cycle during which the probe and the skin were separated. Adding a static pre-indentation to the vibration reduced this fraction, and for this condition a decrease in vibratory amplitude also decreased the fraction. Thus the skin motion contained harmonics that were not present in the probe motion, and the harmonic content differed for different stimulus conditions.

Geometry of rubrospinal, rubroolivary, and local circuit neurons in the macaque red nucleus

The primate red nucleus consists of three main neuron subpopulations, namely, rubrospinal neurons in the magnocellular nucleus, rubroolivary cells in the parvocellular nucleus, and local circuit neurons in both subnuclei: Each subpopulation has unique cerebellar and neocortical inputs. The structural framework for the interactions of these rubral subpopulations remains poorly defined and was the focus of this study in six macaques. Somata of rubrospinal neurons, dorsolateral‐spinal (DL‐spinal) neurons, as defined in the accompanying paper (Burman et al. [2000] J. Comp. Neurol., this issue), and rubroolivary neurons were labeled retrogradely first with Fast Blue injected either into the cervical spinal cord or the inferior olive. The soma/dendrite profiles of selected cells (53 rubrospinal, 19 DL‐spinal, and 17 rubroolivary cells) were visualized by the intracellular injection of Lucifer Yellow/biocytin in fixed slices (400 μm thick) of midbrain. The descriptive statistics of the somata and the dendritic arborization of each rubral neuron type were established. Projection neuron subpopulations had similar but differentiable soma/dendrite profiles, with four to six slender, spine‐bearing dendritic trees radiating out ≈400 μm from the soma. Twelve presumed interneurons, all in the parvocellular nucleus, differed from projection neurons in that they had smaller somata and many slender, spine‐bearing segments that constituted the multibranching dendrite profile that radiated out ≈250 μm from the soma. A tentative model of the macaque rubral microcircuitry was developed, and its functional implications were explored. It incorporated 1) the known topography of the nucleus and its connections, 2) our data specifying the soma/dendrite morphology of the three main rubral neuron types, and 3) the ultrastructure reported by other laboratories of intrarubral synaptic connections. J. Comp. Neurol. 423:197–219, 2000.

Neuron Populations in Sensorimotor Thalamic Space: Connections, Parcellation, and Relation to Corticospinal Projections in the Macaque Monkey

Publisher Summary This chapter examines the connections of the thalamus and sensorimotor cortex that contribute to the channeling and distribution of sensorimotor information, and ultimately relay this information to the spinal cord and musculature. All of the proprioceptive and tactile information specifying hand and finger sensorimotor action, along with that from the cerebellum, basal ganglia, and brainstem, which helps to shape this action, is transmitted to the sensorimotor cortex through the thalamus. The organization of thalamocortical neuron populations mediating this transfer is important, and one analytic approach is to examine how these populations can be functionally compartmentalized on the basis of their extrinsic connections. From the approach, it is found that every part of the sensorimotor cortex receives a complex, convergent, and unique thalamic input. At least six different somatotopically-organized neuron populations in this sensorimotor cortex give origin to direct corticospinal projections to each spinal segment, transmitting in parallel information related to the execution of a particular manual task.

Distribution of Thalamic Input to the Sensorimotor Cortex of the Macaque Monkey

It is a truism that grasping a nearby object with the hand, and examining and identifying its features by touch, is a sensorimotor action of great complexity and sophistication. We cannot use the hand in this way unless the brain receives a continuous inflow of proprioceptive and tactile sensory information, mostly generated by the movement itself, which specifies the position of the hand in space, and the contact it makes with the object. Nor can the sensory information needed to identify the form and surface features of this object be collected efficiently without using the appropriate exploratory movements of the fingers. It has been known for a century that this intelligent, adaptive manual action depends on the integrity of a large wedge of neocortex surrounding the central sulcus of the primate hemisphere, directed movements being determined by precentral cortex, and touch and proprioception requiring minimally an intact postcentral cortex. However, it is still not clear whether the integration of sensory and motor information that underlies the execution of a dextrous manual task, begins first in the sensorimotor cortex, or earlier, in the thalamus. The pattern of thalamocortical projections to the sensorimotor cortex should provide clues to this problem.