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I Darian-Smith

Publications and source records attributed to I Darian-Smith.

At least 19 recordsLinked to original sources

Thalamic projections to areas 3a, 3b, and 4 in the sensorimotor cortex of the mature and infant macaque monkey.

Area 3a in the macaque monkey, located in the fundus of the central sulcus, separates motor and somatosensory cortical areas 4 and 3b. The known connections of areas 4 and 3b differ substantially, as does the information which they receive, process, and transfer to other parts of the central nervous system. In this analysis the thalamic projections to each of these three cortical fields were examined and compared by using retrogradely transported fluorescent dyes (Fast Blue, Diamidino Yellow, Rhodamine and Green latex microspheres) as neuron labels. Coincident labeling of projections to 2-3 cortical sites in each monkey allowed the direct comparison of the soma distributions within the thalamic space of the different neuron populations projecting to areas 3a, 3b, and 4, as well as to boundary zones between these cortical fields. The soma distribution of thalamic neurons projecting to a small circumscribed zone (diameter = 0.5-1.0 mm) strictly within cortical area 3a (in region of hand representation) filled out a "territory" traversing the dorsal half of the cytoarchitectonically defined thalamic nucleus, VPLc (abbreviations as in Olszewski [1952] The Thalamus of the Macaca mulatta. Basel: Karger). This elongate, rather cylindrical, territory extended caudally into the anterior pulvinar nucleus, but not forward into VPLo. The rostrocaudal extent of the thalamic territory defining the soma distribution of neurons projecting to small zones of cortical area 3b was similar, but typically extended into the ventral part of VPLc, filling out a medially concavo-convex laminar space. Two such territories projecting to adjacent zones of areas 3a and 3b, respectively, overlapped and shared thalamic space, but not thalamic neurons. Contrasting with the 3a and 3b thalamic territories, the soma distribution of thalamic neurons projecting to a circumscribed zone in the nearby motor cortex (area 4) did not penetrate into VPLc, but instead filled out a mediolaterally flattened territory extending from rostral VLo, VLm, VPLo to caudal and dorsal VLc, LP, and Pul.o. These territories skirted around VPLc. All three cortical areas 4, 3a, and 3b) also received input from distinctive clusters of cells in the intralaminar Cn.Md. It is inferred that, in combination, the thalamic territories enveloping those neuron somas projecting to, say, the sensorimotor hand representation in areas 3a, 3b, and 4 (and also areas 1 and 2), which would be coactive during the execution of a manual task, constituted a lamellar space extending from VLo rostrally to Pul.o caudally.(ABSTRACT TRUNCATED AT 400 WORDS)

Aging

Ipsilateral cortical projections to areas 3a, 3b, and 4 in the macaque monkey.

In the macaque monkey area 3a of the cerebral cortex separates area 4, a primary motor cortical field, from somatosensory area 3b, which has a subcortical input mainly from cutaneous mechanoreceptive neurons. That each of these cortical areas has a unique thalamic input was illustrated in the preceding paper. In the present experiments the cortical afferent projections to these 3 areas of the sensorimotor cortex monkey were visualized and compared, using 4 differentiable fluorescent dyes as axonal retrogradely transported labels. The cortical projection patterns to areas 3a, 3b, and 4 were similar in that they each consisted of (a) a "halo" of input from the immediately surrounding cortex, and (b) discrete projections from one or more remote cortical areas. However, the pattern of remote inputs from precentral, mesial, and posterior parietal cortex was different for each of the 3 cortical target areas. The cortical input configuration was least complex for area 3b, its remote input projecting mainly from insular cortex. The pattern of discrete cortical inputs to the motor area 4, however, was more complex, with projections from the cingulate motor area (24c/d), the supplementary motor area, postarcuate cortex, insular cortex, and postcentral areas 2/5. Area 3a, in addition to the proximal projections from the immediately surrounding cortex, also received input from the supplementary motor area, cingulate motor cortex, insular cortex, and areas 2/5. Thus, this pattern of cortical input to area 3a resembled more closely that of the adjacent motor rather than that of the somatosensory area 3b. Contrasting with this, however, the thalamic input to area 3a was largely from somatosensory VPLc (abbreviations from Olszewski [1952] The Thalamus of the Macaca mulatta. Basel: Karger) and not from VPLo (with input from cerebellum, and projecting to precentral motor areas).

Aging

Thalamic projections to sensorimotor cortex in the macaque monkey: use of multiple retrograde fluorescent tracers.

We used several fluorescent dyes (Fast Blue, Diamidino Yellow, Rhodamine Latex Microspheres, Evans Blue, and Fluoro-Gold) in each of eight macaques, to examine the patterns of thalamic input to the sensorimotor cortex of macaques 12 months or older. Inputs to different zones of motor, premotor, and postarcuate cortex, supplementary motor area, and areas 3b/1 and 2/5 in the postcentral cortex, were examined. Coincident labeling of thalamocortical neuron populations with different dyes (1) increased the precision with which their soma distributions could be related within thalamic space, and (2) enabled the detection by double labeling, of individual thalamic neurons that were common to the thalamic soma distributions projecting to separate, dye-injected cortical zones. Double-labeled thalamic neurons projecting to sensorimotor cortex were rarely seen in mature macaques, even when the injection sites were only 1-1.5 mm apart, implying that their terminal arborizations were quite restricted horizontally. By contrast, separate neuron populations in each thalamic nucleus with input to sensorimotor cortex projected to more than one cytoarchitecturally distinct cortical area. In ventral posterior lateral (oral) (VPLo), for example, separate populations of cells sent axons to precentral medial, and lateral area 4, medial premotor, and postarcuate cortex, as well as to supplementary motor area. Extensive convergence of thalamic input even to the smallest zones of dye uptake in the cortex (approximately 0.5 mm3) characterized the sensorimotor cortex. The complex forms of these projection territories were explored using 3-dimensional reconstructions from coronal maps. These projection territories, while highly ordered, were not contained by the cytoarchitectonic boundaries of individual thalamic nuclei. Their organization suggests that the integration of the diverse information from spinal cord, cerebellum, and basal ganglia that is needed in the execution of complex sensorimotor tasks begins in the thalamus.

Afferent Pathways

Thalamic projections to sensorimotor cortex in the newborn macaque.

In the present experiments thalamocortical projections to different functional areas of the newborn (or prematurely delivered) macaque's sensorimotor cortex were labeled using retrogradely transported fluorescent dyes. Several dyes were used in each animal to (1) enable the direct comparison of the soma distributions of different thalamocortical projections within thalamic space, and (2) identify by double labeling neurons shared between these distributions. The projection patterns in the newborn macaque were compared with those of the mature animal reported by Darian-Smith et al. (J. Comp. Neurol. 1990;298:000-000). The main observations were (1) all thalamocortical projections to the sensorimotor cortex of the mature macaque are well established by embryonic days 146-150, as was shown by labeling these pathways in infants delivered by cesarean section, (2) a significant number of thalamocortical neurons in the newborn were double-labeled following dye injections into different pre- or postcentral areas, and where the margins of the dye uptake zones were separated by 3-8 mm, and (3) extensive projections from the anterior pulvinar nucleus to the motor and premotor cortex, and to the supplementary motor cortex were labeled in the newborn macaque. Both the exuberant terminal arborizations, and the precentral pulvinar projections were diminished by the 6th postnatal month, and absent in the mature macaque. The role of epigenetic determinants of these postnatal events is briefly considered.

Afferent Pathways

Tactile discrimination of thickness.

The ability of human subjects to discriminate plane metal plates of different thickness was measured using of 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 in 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 degrees.

Adult

Skin profiles during sinusoidal vibration of the fingerpad.

Skin 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.

Animals

Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad.

Gratings of alternating grooves and ridges were moved sinusoidally across the fingerpads of anesthetized monkeys, while responses were recorded from individual slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) in the median nerve. The stimulus comprised 2 spatial variables, namely, groove width (G) and ridge width (W), and 2 temporal variables, namely, the peak speed of movement (S) and the peak temporal frequency (F) at which successive spatial cycles of the grating pass over a point in the receptive field. The responses of all 3 fiber types were determined by only 1 spatial variable, G, and only 1 temporal variable, F. Changes in W or S affected responses only if there was a concomitant change in either G or F. Responses were phase-locked to the occurrence of successive spatial cycles of the grating, and we have used the number of impulses elicited by a single spatial cycle as the fundamental measure of response. An equation of the form I = cGaexp(-b square root of F) describes the responses of all 3 fiber types. For SAs, the effect of groove width was greater (a = 2.64) than for RAs and PCs (a = 0.924 and 1.05, respectively). The reduction in response with frequency was most marked for SAs (b = 0.262), and greater for PCs (b = 0.167) than for RAs (b = 0.130). From the equation, the instantaneous response during the entire sinusoidal cycle was reconstructed as well as a second measure, the mean cyclic response. These 2 measures behaved differently with changes in the stimulus parameters. The temporal properties of the fibers, as revealed by gratings, may appear to be in conflict with those established by vibratory threshold studies; in fact, they are compatible with suprathreshold responses to vibrating probes.

Animals

Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad.

Human subjects scaled gratings of alternating grooves and ridges for perceived roughness. Roughness increased with an increase in groove width and decreased with an increase in ridge width, but the effect of groove width was much greater than the effect of ridge width. In corresponding neurophysiological experiments, the gratings were moved sinusoidally across the receptive fields of single mechano-receptive afferents innervating the fingerpads of anesthetized monkeys. The measure of response used was the mean cyclic discharge rate (averaged over one cycle of the sinusoid). Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) all showed a marked increase in response when groove width increased. An increase in ridge width had no consistent effect on the responses of SAs or RAs but resulted in a small decrease in the response of PCs. The response to a smooth surface differed significantly from the responses to the finer gratings only for the RAs. An alternative measure of response (the number of impulses elicited by each spatial cycle of the grating) increased with an increase in ridge width for all 3 fiber types. Thus, the large effect of groove width on perceived roughness can be accounted for by the mean cyclic discharge rate in the active afferent fibers. The smaller effect of ridge width can be accounted for by the number of impulses per spatial cycle of the grating.

Adult

A stimulator for moving textured surfaces sinusoidally across the skin.

The stimulator allows textured surfaces to be moved sinusoidally across the skin of the fingerpad. Sinusoidal motion is produced by a "scotch yolk" driven by a DC motor. The amplitude of movement is adjustable up to a maximum of 80 mm peak to peak and the frequency is continuously adjustable from 0.1 Hz to 2.0 Hz. Movement of the surface is monitored by an optical transducer and contact force between the finger and the surface is monitored by a strain gauge bridge. The stimulator is simple and robust and is suitable for both neurophysiological and psychophysical experiments in animals and humans.

Animals

Tactile discrimination of gratings.

Human 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 mu, 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.

Adolescent

Transcutaneous recording of single neuron activity in the cerebral cortex of the monkey.

A new method is described for recording responses of single neurons in the monkey's cerebral cortex by passing a microelectrode directly through the overlying skin and dura. Previous to this recording a window had been cut in the calvarium, and the bone deficit repaired using a full-thickness skin graft. Stable unitary recordings have been made over a period of one year following craniotomy, the only skull attachment being a small stainless steel peg, on which the microdrive was mounted when required.

Animals

Touching textured surfaces: cells in somatosensory cortex respond both to finger movement and to surface features.

Single neurons in Brodmann's areas 3b and 1 of the macaque postcentral gyrus discharge when the monkey rubs the contralateral finger pads across a textured surface. Both the finger movement and the spatial pattern of the surface determine this discharge in each cell. The spatial features of the surface are represented unambiguously only in the responses of populations of these neurons, and not in the responses of the constitutent cells.

Animals

Touch in primates.

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Afferent Pathways

Peripheral neural representation of the spatial frequency of a grating moving across the monkey's finger pad.

1. Responses in mechanoreceptive afferent fibres innervating the monkey's finger pads were examined when a ridged surface ("grating') was moved across the fibre's receptive field with a specified velocity and applied force. 2. The stimulus feature represented in single fibre responses was the temporal frequency of the moving grating (stimulus temporal frequency = velocity of moving surface/spatial period); information about the spatial period of the grating was represented equivocally. 3. Peripheral neural representation of the grating's spatial period (or spatial frequency) depended on information signalled by the responding fibre population rather than by individual fibres. 4. The three mechanoreceptive fibre populations responded differentially to a grating moving across the finger pad. Slowly adapting fibres coded best those stimulus combinations with a stimulus temporal frequency in the range 20-60 Hz, rapidly adapting fibres coded best those with frequencies of 60-200 Hz, and Pacinian fibres best defined those stimuli with a high temporal frequency (100-300 Hz). 5. Applying the moving grating to the skin with varying radial forces in the range 20-60 g wt. did not greatly modify the pattern of discharge in the responding fibre populations.

Action Potentials

Peripheral neural representation of spatial dimensions of a textured surface moving across the monkey's finger pad.

1. The responses of single cutaneous mechanoreceptive fibres evoked by a geometrically patterned surface sweeping across the skin were examined. The surfaces used were each a fine diamond-shaped array of "dots' in relief against a flat background. The fibres examined were rapidly adapting, slowly adapting and Pacinian fibres innervating the monkey's finger pad skin. 2. Each fibre's response to the two-dimensioned surface was assessed using a procedure in which the surface was swept across the fibre's receptive field many times, the position of the surface relative to the underlying receptive field being precisely known at any instant in time. Between each successive sweep the stimulus surface was shifted lateral to the direction of movement by a small increment. The response pattern generated by this scanning procedure specified the extent to which a single response of the fibre was dependent on the spatial and temporal dimensions of the stimulus. 3. The invariant spatial features of the moving surface were represented only in the responses of populations of fibres; responses of the constituent fibres always confounded the information relayed about the surface pattern and its rate of movement across the skin. 4. Factors determining the representation of the spatial and temporal characteristics of the moving surface in the responding mechanoreceptive fibre population were examined. These included the response characteristics of the constituent fibres, the innervation density, and the total number of fibres engaged by the moving surface.

Action Potentials

Innervation density of mechanoreceptive fibres supplying glabrous skin of the monkey's index finger.

1. The innervation densities of mechanoreceptive fibres supplying the ridged glabrous skin of the middle and terminal phalanges of the monkey's (Macaca nemestrina) index finger were estimated using a combination of histological and neurophysiological procedures. 2. This estimate was based on (a) a count of the total number of A beta myelinated fibres in the palmar digital nerve at the level of the proximal phalanx, (b) the demonstration that the majority of A beta fibres in the monkey's palmar digital nerve are mechanoreceptive afferents, (c) the estimation, based on a sample of 398 fibres, of the fractions of rapidly adapting, slowly adapting and Pacinian mechanoreceptive fibres in the palmar digital nerve, and (d) the estimation of the area of glabrous skin innervated by the palmar digital nerve. 3. The estimated innervation density of the finger pad and the skin of the middle phalanx were: rapidly adapting fibres, 178 and 80/cm2; slowly adapting fibres, 134 and 46/cm2; and Pacinian fibres, 13/cm2 for both phalanges.

Animals

Warm fibers innervating palmar and digital skin of the monkey: responses to thermal stimuli.

1. Three hundred fourteen warm fibers innervating the glabrous skin of the monkey's hand were isolated by dissection in the median and ulnar nerves in two species, Macaca mulatta and M. nemestrina. Fiber samples in the two species were functionally similar and uniform in their properties. Their mean conduction velocity of 1.2 m/s (SD 0.5; n = 50) implies that these warm fibers were all unmyelinated. 2. A parametric study of the responses of warm fibers to near-rectangular warming and cooling pulses applied to glabrous skin was completed using 104 fibers. At a steady base-line skin temperature (T-base) of 34 degrees C all these warm fibers responded to warming pulses in the intensity range 0--8 degrees C with a simple, uniform discharge, which reached a peak rate of 1.5--4.0 s after the onset of stimulation; subsequent decay in this discharge rate had a time constant of 5--12 s and was virtually independent of the intensity of the warm pulse. The intensity function was linear for most fibers when the interstimulus interval was 60 s or longer. At a T-base of 29 degrees C, warm fibers were less responsive, but the temporal profile of the response was similar to that at a T-base of 34 degrees C in the intensity range 4--8 degrees C, and the intensity function was again linear. 3. At a T-base of 39 degrees C the intensity function of each warm fiber was complex. Most fibers responded briskly to warming pulses of 2--4 degrees C: the response to more intense warming pulses, particularly when the skin temperature rose above 45 degrees C, was structured and reproducible, but varied greatly among different fibers. With some the discharge evoked was of very high frequency for a few seconds, and then ceased. More than 80% of the sample of warm fibers did not discharge at all in response to warming pulses, which raised the skin temperature to 50 degrees C or above. 4. The responsiveness of warm fibers to warming pulses was dependent on previous stimulation when the interstimulus interval was less than 60 s. This temporal suppression was precisely structured and was examined quantitatively for trains of warming pulses, each lasting 4.0 s and presented every 10 s. The pattern of suppressive interaction was similar in form to that previously reported for cold fibers innervating palmar skin. 5. A quantitative study of the receptive fields of individual warm fibers demonstrated a spatiotemporal response pattern, which is best described in terms of a focal receptor zone less than 1 mm in diameter surrounded by thermally conducting skin. The skin's thermal conductivity is paramount in determining the warm-fiber's receptive-field characteristics. 6. The responses of warm fibers to cooling pulses and to warming ramps are described.

Animals