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C J Bruce

Publications and source records attributed to C J Bruce.

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Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex.

1. Single-neuron activity was recorded from the prefrontal cortex of monkeys performing saccadic eye movements in oculomotor delayed-response (ODR) and visually guided saccade (VGS) tasks. In the ODR task the monkey was required to maintain fixation of a central spot throughout the 0.5-s cue and 3.0-s delay before making a saccadic eye movement in the dark to one of four or eight locations where the visual cue had been presented. The same locations were used for targets in the VGS tasks; however, unlike the ODR task, saccades in the VGS tasks were visually guided. 2. Among 434 neurons recorded from prefrontal cortex within and surrounding the principal sulcus (PS), 147 changed their discharge rates in relation to saccadic eye movements in the ODR task. Their response latencies relative to saccade initiation were distributed between -192 and 460-ms, with 22% exhibiting presaccadic activity and 78% exhibiting only postsaccadic activity. Among PS neurons with presaccadic activity, 53% also had postsaccadic activity when the monkey made saccadic eye movements opposite to the directions for which the presaccadic activity was observed. 3. Almost all (97%) PS neurons with presaccadic activity were directionally selective. The best direction and tuning specificity of each neuron were estimated from parameters used to fit a Gaussian tuning curve function. The best direction for 62% of the neurons with presaccadic activity was toward the contralateral visual field, with the remaining neurons having best directions toward the ipsilateral field (23%) or along the vertical meridian (15%). 4. Most postsaccadic activity of PS neurons (92%) was also directionally selective. The best direction for 48% of these neurons was toward the contralateral visual field, with the remaining neurons having best directions toward the ipsilateral field (36%) or along the vertical meridian (16%). Eighteen percent of the neurons with postsaccadic activity showed a reciprocal response pattern: excitatory responses occurred for one set of saccade directions, whereas inhibitory responses occurred for roughly the opposite set of directions. 5. Sixty PS neurons with saccade-related activity in the ODR task were also examined in a VGS task. Forty of these neurons showed highly similar profiles of directional specificity and response magnitude in both tasks, 13 showed saccade-related activity only in the ODR task, and 7 changed their response characteristics between the ODR and VGS tasks.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms.

1. Visual responses and their relationship to delay-period activity were studied by recording single neuron activity from the prefrontal cortex of rhesus monkeys while they performed an oculomotor delayed-response (ODR) and a visual probe (VP) task. In the ODR task, the monkey was required to maintain fixation of a central spot of light throughout the cue (0.5 s) and delay (3 s) periods and then make a saccadic eye movement to one of four or eight locations where the visual cue had been presented. In the VP task, the same visual stimuli that were used in the ODR task were presented for 0.5 s, but no response was required. The VP task was thus employed to test the passive visual response and, by comparison with cue-elicited activity in the ODR task, to examine the degree of behavioral enhancement present in prefrontal visual activity. 2. Among 434 neurons recorded from the prefrontal cortex within and surrounding the principal sulcus (PS), 261 had task-related activity during at least one phase of the ODR task, and 74 of these had phasic visual responses to the onset of the visual cues with a median latency of 116 ms. The visual responses of 69 neurons were excitatory, and 5 neurons were inhibited. Five of the neurons with excitatory visual responses also responded transiently after the offset of the cue. 3. Visual responses were classified as directional for 71 PS neurons (96%) in that excitatory or inhibitory responses occurred only for location of cues in a restricted portion of the visual field. Only 3 PS neurons were omnidirectional, i.e., responded equivalently to cues in all locations tested. 4. The best direction and tuning specificity of all PS neurons with directional visual responses were estimated from parameters yielding the best fit to a Gaussian-shaped tuning function. The best direction for the majority (71%) of neurons was toward the visual field contralateral to the hemisphere where the neuron was located. The remaining neurons had their best directions in the ipsilateral field (18%) or along the vertical meridian (11%). 5. The specificity of directional tuning for PS visual responses was quite variable, ranging from neurons that responded only to one of the eight cue locations to neurons that responded to all eight, but in a clearly graded fashion. The standard deviation parameter of the Gaussian curve indexed the breadth of directional tuning of each neuron; its median value was 37 degrees.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal.

1. We studied the activity of single neurons in the monkey frontal eye fields during oculomotor tasks designed to assess the activity of these neurons when there was a dissonance between the spatial location of a target and its position on the retina. 2. Neurons with presaccadic activity were first studied to determine their receptive or movement fields and to classify them as visual, visuomovement, or movement cells with the use of the criteria described previously (Bruce and Goldberg 1985). The neurons were then studied by the use of double-step tasks that dissociated the retinal coordinates of visual targets from the dimensions of saccadic eye movements necessary to acquire those targets. These tasks required that the monkeys make two successive saccades to follow two sequentially flashed targets. Because the second target disappeared before the first saccade occurred, the dimensions of the second saccade could not be based solely on the retinal coordinates of the target but also depended on the dimensions of the first saccade. We used two versions of the double-step task. In one version neither target appeared in the cell's receptive or movement field, but the second eye movement was the optimum amplitude and direction for the cell (right-EM/wrong-RF task). In the other the second stimulus appeared in the cell's receptive field, but neither eye movement was appropriate for the cell (wrong-EM/right-RF task). 3. Most frontal-eye-field cells discharged in the right-EM/wrong-RF version of the double-step task. Their discharge began after the first saccade and continued until the second saccade was made. They usually discharged even on occasional trials in which the monkey failed to make the second saccade. They discharged much less, or not at all, in the wrong-EM/right-RF version of the double-step paradigm. Thus most presaccadic cells in the frontal eye fields were tuned to the dimensions of saccadic eye movements rather than to the coordinates of retinal stimulation. 4. Eleven movement cells (including 1 which also had independent postsaccadic activity for saccades opposite its presaccadic movement field) were studied, and all had significant activity in the right-EM/wrong-RF task. 5. Almost all (28/32) visuomovement cells, including 12 with independent postsaccadic activity, discharged in the right-EM/wrong-RF task. None of the four that failed had independent postsaccadic activity. 6. The majority (26/40) of visual cells were responsive in the right-EM/wrong-RF task.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex.

1. An oculomotor delayed-response task was used to examine the spatial memory functions of neurons in primate prefrontal cortex. Monkeys were trained to fixate a central spot during a brief presentation (0.5 s) of a peripheral cue and throughout a subsequent delay period (1-6 s), and then, upon the extinction of the fixation target, to make a saccadic eye movement to where the cue had been presented. Cues were usually presented in one of eight different locations separated by 45 degrees. This task thus requires monkeys to direct their gaze to the location of a remembered visual cue, controls the retinal coordinates of the visual cues, controls the monkey's oculomotor behavior during the delay period, and also allows precise measurement of the timing and direction of the relevant behavioral responses. 2. Recordings were obtained from 288 neurons in the prefrontal cortex within and surrounding the principal sulcus (PS) while monkeys performed this task. An additional 31 neurons in the frontal eye fields (FEF) region within and near the anterior bank of the arcuate sulcus were also studied. 3. Of the 288 PS neurons, 170 exhibited task-related activity during at least one phase of this task and, of these, 87 showed significant excitation or inhibition of activity during the delay period relative to activity during the intertrial interval. 4. Delay period activity was classified as directional for 79% of these 87 neurons in that significant responses only occurred following cues located over a certain range of visual field directions and were weak or absent for other cue directions. The remaining 21% were omnidirectional, i.e., showed comparable delay period activity for all visual field locations tested. Directional preferences, or lack thereof, were maintained across different delay intervals (1-6 s). 5. For 50 of the 87 PS neurons, activity during the delay period was significantly elevated above the neuron's spontaneous rate for at least one cue location; for the remaining 37 neurons only inhibitory delay period activity was seen. Nearly all (92%) neurons with excitatory delay period activity were directional and few (8%) were omnidirectional. Most (62%) neurons with purely inhibitory delay period activity were directional, but a substantial minority (38%) was omnidirectional. 6. Fifteen of the neurons with excitatory directional delay period activity also had significant inhibitory delay period activity for other cue directions. These inhibitory responses were usually strongest for, or centered about, cue directions roughly opposite those optimal for excitatory responses.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Resolution of metabolic columns by a double-label 2-DG technique: interdigitation and coincidence in visual cortical areas of the same monkey.

A double-label modification of the 2-deoxyglucose (DG) technique uses both 3H-2-DG and 14C-2-DG and allows for metabolic activity engaged by 2 distinct experimental conditions to be dissociated throughout the brain of a single subject. In the present study, we used this double-label method to examine the relationship between metabolic columns subserving the 2 eyes in cortical visual areas V1 and V2. The left and right eye's ocular dominance columns were separately activated in the same monkey to demonstrate that the double-label 2-DG method can resolve metabolic differences at the level of the cortical column. In 2 monkeys, 14C-2-DG was injected first and one eye was occluded while the other eye was visually stimulated for 30 min. Then 3H-2-DG was injected, and the occluder was switched so that the alternate eye was stimulated with the same pattern for 30 min. Autoradiographs depicting the 2 labels separately were obtained by exploiting the differential sensitivity of X-ray film and Ultrofilm to 3H and 14C emissions and by applying a radioactivity-subtraction algorithm to pairs of digitized images of the same section (Friedman et al., 1987). Columnar regions of increased activity were evident throughout V1, excepting the representations of the optic disk and monocular crescent. Superimposition of the 3H and 14C images from the same sections demonstrated that columns of increased 3H label were interdigitated with columns of increased 14C label in V1. In contrast, bands of increased 3H-2-DG uptake in extrastriate area V2 were largely coincident with the bands of increased 14C-2-DG uptake. These results illustrate the value of the double-label 2-DG technique for studying fluctuations of metabolic activity under different experimental conditions in the same subject. In the present example, the demonstration that ocular dominance columns are interdigitated in V1, whereas metabolically active bands are coincident in V2, would not have been fully appreciated by comparing 2-DG labeling across separate animals.

Animals

Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields.

Anterograde tracers (tritiated leucine, proline, fucose; WGA-HRP) were injected into sites within the frontal eye fields (FEF) of nine macaque monkeys. Low thresholds (less than or equal to 50 microA) for electrically evoking saccadic eye movements were used to locate injection sites in four monkeys. Cases were grouped according to the amplitude of saccades evoked or predicted at the injection site. Dorsomedial prearcuate injection sites where large saccades were elicited were classified as lFEF cases, whereas ventrolateral prearcuate sites where small saccades were evoked were designated sFEF cases. One control case was injected in the medial postarcuate area 6. We found five descending fiber bundles from FEF; fibers to the striatum, which enter the caudate nucleus at or just rostral to the genu of the internal capsule; fibers to the claustrum, which travel in the external capsule; and transthalamic, subthalamic, and pedunculopontine fibers. Our results indicate that transthalamic and subthalamic pathways supply all terminal sites in the thalamus, subthalamus, and tegmentum of the midbrain and pons, whereas pedunculopontine fibers appear to terminate in the pontine and reticularis tegmenti pontis nucleus exclusively. Frontal eye field terminal fields in the striatum were topographically organized: lFEF projections terminated dorsal and rostral to sFEF projections. Thus, lFEF terminal fields were located centrally in the head and body of the caudate nucleus and a small dorsomedial portion of the putamen, whereas sFEF terminal fields were located in ventrolateral parts of the caudate body and ventromedial parts of the putamen. In the claustrum, lFEF projections terminated dorsal and rostral to sFEF projections. Projections from FEF terminated in ventral and caudal parts of the subthalamic nucleus without a clear topography. By comparison, terminal fields from medial postarcuate area 6 were located more caudally and laterally in the striatum and claustrum than projections from FEF, and more centrally in the subthalamic nucleus. In the thalamus, FEF terminal patches in some thalamic nuclei were also topographically organized. Projections from lFEF terminated in dorsal area X, dorsolateral medial dorsal nucleus, pars parvicellularis (MDpc), and the caudal pole of MDpc, whereas projections from sFEF terminated in ventral area X, medial dorsal nucleus, pars multiformis, and caudal medial dorsal nucleus pars densocellularis.(ABSTRACT TRUNCATED AT 400 WORDS)

Amino Acids

Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons.

Frontal eye field (FEF) projections to the midbrain and pons were studied in nine macaque monkeys that were used to study FEF projections to the striatum and thalamus (Stanton et al.: J. Comp. Neurol. 271:473-492, '88). Injections of tritiated amino acids or WGA-HRP were made into FEF cortical locations where low-level microstimulation (less than or equal to 50 microA) elicited saccadic eye movements, and anterograde axonal labeling was mapped. The injections were made into the anterior bank of the arcuate sulcus from dorsomedial sites where large saccades were evoked (lFEF) to ventrolateral sites where small saccades were evoked (sFEF). The largest terminal fields of FEF fibers were located in the ipsilateral superior colliculus (SC). Projections to SC were topographically organized: lFEF sites projected to intermediate and deep layers of caudal SC, sFEF sites projected to intermediate and superficial layers of rostral SC, and FEF sites between these extremes projected to intermediate locations in SC. Patches of terminal labeling were located ipsilaterally in the lateral mesencephalic reticular formation near the parabigeminal nucleus and the ventrolateral pontine reticular formation. These patches were larger from lFEF injections. Small, dense terminal patches were seen in the ipsilateral pontine gray, mostly along the medial and dorsal borders of these nuclei but occasionally in central and dorsolateral regions. Patches of label like those in the pontine nuclei were located ipsilaterally in the reticularis tegmenti pontis nucleus in lFEF cases and bilaterally in sFEF cases. Small terminal patches were found in the nucleus of Darkschewitsch and dorsal and medial parts of the parvicellular red nucleus in most FEF cases. In the pretectal region, labeled terminal patches were consistently found in the nucleus limitans of the posterior thalamus, but we could not determine if label in the nucleus of the pretectal area and dorsal parts of the nucleus of the posterior commissure marked axon terminals or fibers of passage. We found small, lightly labeled terminal patches in the pontine raphe between the rootlets of the abducens nerve (three cases) or in the adjacent paramedian pontine reticular formation (one case). Omnipauser cells in this region are important in initiating saccades. In one sFEF case, very small patches of label were located in the supragenual nuclei anterior to the abducens nuclei and in the ipsilateral nucleus prepositus hypoglossi posterior to the abducens nucleus. Presaccadic burster neurons in the periabducens region are known to fire immediately before horizontal saccades.(ABSTRACT TRUNCATED AT 400 WORDS)

Amino Acids

A sequential double-label 14C- and 3H-2-DG technique: validation by double-dissociation of functional states.

We investigated a double-label 2-DG protocol and method of analysis in which sequential injections of 3H- and 14C-2-DG were used to map brain metabolism during two distinct experimental treatments in the same animal. In initial studies, brain sections from rats given only 3H-2-DG or only 14C-2-DG were exposed on Ultrofilm and on X-ray film with an interposed sheet of mylar (X-ray/mylar). These studies were needed to determine whether, at the 50:1 3H:14C dose ratio used, 3H-2-DG uptake would be revealed only in Ultrofilm images and 14C-2-DG uptake only in X-ray/mylar images. We found that X-ray/mylar images indeed showed only 14C-2-DG uptake as 3H emissions were blocked by the protective coating of the film and the mylar. By contrast, Ultrofilm autoradiograms showed the 2-DG uptake pattern for both the 14C-2-DG and 3H-2-DG cases. We then examined autoradiograms from double-label cases in which 14C-2-DG and 3H-2-DG were sequentially given using a 100:1 3H:14C dose ratio, with a different treatment following each injection. As predicted from the single-label cases, activity in the X-ray/mylar images corresponded to the treatment that followed the 14C-2-DG injection, while the Ultrofilm images reflected both treatments and thus were not veridical representations of 3H label. This paper provides a solution to the contamination of Ultrofilm by 14C label in that we devised a subtraction algorithm using a computerized imaging system which removes the contaminating 14C from the Ultrofilm image, leaving a 'Difference' image of 3H-2-DG uptake. Difference images revealed activity consistent with the treatment that followed the 3H-2-DG injection. Thus, the X-ray/mylar and difference images separately indexed metabolic activity for two different functional states in the same subject. By allowing a subject to serve as its own control, this double-label method greatly increases the applicability and power of the 2-DG method.

Algorithms

The role of striate cortex in the guidance of eye movements in the monkey.

We studied the effect of unilateral striate cortical ablations on smooth pursuit and saccadic eye movements in the monkey. The monkeys made quite accurate saccades to stationary stimuli in the field contralateral to the lesion, and they readily pursued foveal targets moving in all directions. However, when visual stimuli were stepped into the field contralateral to the lesion and then began to move, thus insuring that the moving stimulus was confined to the impaired visual hemifield, several oculomotor abnormalities emerged. Saccades to moving stimuli presented in the impaired field consistently undershot targets that moved away from the central fixation point after the step, and overshot targets that moved back towards the central fixation point. There was little or no smooth pursuit eye velocity generated in any direction to moving stimuli in the impaired field, and the monkeys could not generate smooth pursuit to stimuli maintained a few degrees from the fovea in the impaired field, although they were able to pursue such stimuli held in the normal field. Ablation of striate cortex also affected the latencies of saccades. When step-ramp stimuli were presented in the normal field, the monkeys delayed the initiation of saccades to targets moving towards the central fixation point, and hastened the initiation of saccades to targets moving away from the central fixation point. By contrast, changes in the direction of target movement did not affect the latencies of saccades into the impaired field. The deficits seemed permanent, lasting as long as the monkeys were tested--over 2 years in one case--but they were not total. Each monkey could use stimuli moving into the affected field to develop some eye velocity, although this residual ability had a much longer latency and lower gain than that provided by the intact visual system. These results show that striate cortex is intimately involved in the estimation of stimulus velocity critical to the genesis of smooth pursuit and saccadic eye movements.

Animals

Both striate cortex and superior colliculus contribute to visual properties of neurons in superior temporal polysensory area of macaque monkey.

Although the tectofugal system projects to the primate cerebral cortex by way of the pulvinar, previous studies have failed to find any physiological evidence that the superior colliculus influences visual activity in the cortex. We studied the relative contributions of the tectofugal and geniculostriate systems to the visual properties of neurons in the superior temporal polysensory area (STP) by comparing the effects of unilateral removal of striate cortex, the superior colliculus, or of both structures. In the intact monkey, STP neurons have large, bilateral receptive fields. Complete unilateral removal of striate cortex did not eliminate visual responses of STP neurons in the contralateral visual hemifield; rather, nearly half the cells still responded to visual stimuli in the hemifield contralateral to the lesion. Thus the visual properties of STP neurons are not completely dependent on the geniculostriate system. Unilateral striate lesions did affect the response properties of STP neurons in three ways. Whereas most STP neurons in the intact monkey respond similarly to stimuli in the two visual hemifields, responses to stimuli in the hemifield contralateral to the striate lesion were usually weaker than responses in the ipsilateral hemifield. Whereas the responses of many STP neurons in the intact monkey were selective for the direction of stimulus motion or for stimulus form, responses in the hemifield contralateral to the striate lesion were not selective for either motion or form. Whereas the median receptive field in the intact monkey extended 80 degrees into the contralateral visual field, the receptive fields of cells with responses in the contralateral field that survived the striate lesions had a median border that extended only 50 degrees into the contralateral visual field. Removal of both striate cortex and the superior colliculus in the same hemisphere abolished the responses of STP neurons to visual stimuli in the hemifield contralateral to the combined lesion. Nearly 80% of the cells still responded to visual stimuli in the hemifield ipsilateral to the lesion. Unilateral removal of the superior colliculus alone had only small effects on visual responses in STP. Receptive-field size and visual response strength were slightly reduced in the hemifield contralateral to the collicular lesion. As in the intact monkey, selectivity for stimulus motion or form were similar in the two visual hemifields. We conclude that both striate cortex and the superior colliculus contribute to the visual responses of STP neurons. Striate cortex is crucial for the movement and stimulus specificity of neurons in STP.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Binocular differences in cortical receptive fields of kittens after rotationally disparate binocular experience.

Kittens were afforded visual experience only while wearing goggles fitted with prisms that rotated the inputs to the two eyes equally but in opposite directions about the visual axes (16 degrees for experimental subjects, 0 degrees for control subjects). Subsequently, receptive-field organization of the visual cortex was studied, special attention being given to the preferred orientation centered about the prism rotation experienced during early development. Thus, for moderate amounts of relative rotation, the development of interocular matching of orientation specificity in binocular cells of the visual cortex reflects the correspondence of early visual input between the two eyes.

Animals

Smooth-pursuit eye movement representation in the primate frontal eye field.

Physiological and behavioral data reported here show an involvement of the primate frontal eye field (FEF) cortex in smooth-pursuit eye movements, in addition to its well-established role in saccadic eye movements. Microstimulation just ventral to the small saccade representation of the FEF elicits eye movements that, in contrast to elicited saccades, have low velocities, continue smoothly without interruption during prolonged stimulation, and are usually directed ipsilaterally to the stimulated hemisphere. Neurons in this region respond in association with smooth-pursuit eye movements and visual motion. Tracking deficits following experimental lesions of the FEF depend critically upon the status of this ventral region: superficial lesions sparing it leave smooth-pursuit eye movements intact, whereas lesions removing it produce substantial deficits in the anticipatory initiation, motion-induced acceleration, asymptotic velocity, and predictive continuation of ipsilateral smooth pursuit.

Animals

Joyce's journey.

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Adolescent