Neuronal activity in motor cortical areas reflects the sequential context of movement

Natural actions can be described as chains of simple elements, whereas individual motion elements are readily concatenated to generate countless movement sequences. Sequence-specific neurons have been described extensively, suggesting that the motor system may implement temporally complex motions by using such neurons to recruit lower-level movement neurons modularly. Here, we set out to investigate whether activity of movement-related neurons is independent of the sequential context of the motion. Two monkeys were trained to perform linear arm movements either individually or as components of double-segment motions. However, comparison of neuronal activity between these conditions is delicate because subtle kinematic variations generally occur within different contexts. We therefore used extensive procedures to identify the contribution of variations in motor execution to differences in neuronal activity. Yet, even after application of these procedures we find that neuronal activity in the motor cortex (PMd and M1) associated with a given motion segment differs between the two contexts. These differences appear during preparation and become even more prominent during motion execution. Interestingly, despite context-related differences on the single-neuron level, the population as a whole still allows a reliable readout of movement direction regardless of the sequential context. Thus the direction of a movement and the sequential context in which it is embedded may be simultaneously and reliably encoded by neurons in the motor cortex.     

Neuronal and behavioral correlations in the medial prefrontal cortex and nucleus accumbens during cocaine self-administration by rats

Up to 31 neurons per animal were simultaneously recorded from the medial prefrontal cortex and nucleus accumbens in 15 rats during i.v. cocaine self-administration sessions, using a multi-channel, single-unit recording technique. Alterations of neuronal activity (both excitatory and inhibitory) were found a few seconds before each lever press for cocaine infusion; we have called these pre-lever press neuronal activations "anticipatory responses". A detailed video analysis revealed that these neuronal firing alterations were associated with specific portions of the behavioral sequence performed before each lever press in both recording areas. Some of the simultaneously recorded neurons displayed similar firing patterns in relation to a given behavioral episode within the behavioral sequence (turning, raising head, etc.), while others fired at different times relative to each behavioral event. Cross-correlational analyses revealed inter-regional and intra-regional correlated firing patterns between pairs of simultaneously recorded medial prefrontal cortex and nucleus accumbens neurons. This correlated firing occurred in the neurons with and without anticipatory responses, although the incidence of correlations between anticipatory neuron pairs was much higher than that between non-anticipatory neuron pairs (18.4% vs 3.6%). Many correlated neuron pairs displayed a time lag in the peak of correlational activity that indicated a temporal sequence in correlated activity. In contradiction to our hypothesis, the temporal pattern of correlation reveals that there are more cases in which nucleus accumbens neurons fired ahead of medial prefrontal cortex neurons.The results suggest that multiple mesocorticolimbic neuronal circuits may code sequential steps during the behavioral sequence performed to obtain an infusion of cocaine. The observed correlated firing between the medial prefrontal cortex and the nucleus accumbens indicates that dynamic, coherent activity occurs within the mesocorticolimbic circuit. Because this circuit is hypothesized to drive drug-seeking behavior, we suggest that this correlated firing between the nucleus accumbens and the medial prefrontal cortex may participate in the control of cocaine self-administration. In addition, the finding that correlated activity within the nucleus accumbens more often precedes that of the medial prefrontal cortex suggests that the nucleus accumbens may play a prime role in the initiation of cocaine self-administration.     

Cue-evoked encoding of movement planning and execution in the rat nucleus accumbens

The nucleus accumbens is involved in the modulation of motivated behaviour by reward-associated sensory information. However, little is known about the specific nature of the nucleus accumbens' contribution to generating movement. We investigated motor encoding by nucleus accumbens neurons in rats performing a delayed response task that allowed us to dissociate the effects of sensory and motor events on firing. In a subset of neurons, firing in the delay period preceding movement was highly selective; this selectivity was tightly correlated with the direction of the subsequent movement, but not with the sensory properties of the instructive cue. Direction selectivity in this population of neurons developed over the course of the delay period, with the strongest selectivity apparent just prior to movement onset. Selectivity was also apparent in nucleus accumbens neurons during movement, such that firing showed a tight correlation with movement direction, but not the instructive cue presented nor the spatial destination of the movement. These results are consistent with the hypothesis that a subpopulation of nucleus accumbens neurons contributes to the selection and execution of specific motivated behaviours.     

Movement-related activity of thalamic neurons with input from the globus pallidus and projection to the motor cortex in the monkey

Summary Thalamic neurons projecting to the arm area of the motor cortex were identified by their antidromic response to stimulation of that area in two awake monkeys. Neurons were further identified as receiving inputs from the cerebellar nuclei or the internal segment of the globus pallidus by excitatory or inhibitory response to stimulation of these nuclei. Most (33/34) of the thalamic neurons in the cerebello-thalamo-cortical projection and more than half (12/18) of those in the pallido-thalamocortical projection changed their firing rate on the leverlifting hand movement in the reaction-time task. A considerable number of neurons of both groups (14/23 and 3/10) changed their firing rate prior to the onset of the earliest EMG. These findings agree with the model that activities of pallidal as well as cerebellar nuclear neurons related to motor control are transmitted to the motor cortex through the thalamus.     

Spike firing in the lateral cerebellar cortex correlated with movement and motor parameters irrespective of the effector limb

Neuronal signals in the lateral aspect of the macaque cerebellar cortex were studied during a visually guided reaching task. During the performance of this task, the firing rate of most neurons was significantly modulated when reaching with either the ipsilateral or the contralateral arm. In some of these reach-modulated cells, we found that spike firing was correlated with the direction and speed of the reach. These correlations with motor parameters were present during reaching with either the ipsilateral or the contralateral arm. Based on these observations we suggest that spike firing in the lateral cerebellum was correlated with movement and motor parameters irrespective of the effector limb.     

Selective coding of motor sequence in the supplementary motor area of the monkey cerebral cortex

Summary We describe a property of neurons in the supplementary motor area (SMA) of the cerebral cortex of monkey that is different from those in the primary motor area (MI) in relation to execution of a sequential motor task. A group of SMA neurons was active when the animal remembered and pressed three touch-pads in a predetermined sequence but inactive when the same movement was guided by sequentially presented visual signals. This finding indicates that the SMA is involved in the performance of sequential movements on the basis of the information stored inside the brain.     

Involvement of human thalamic neurons in internally and externally generated movements

Several anatomical studies support the existence of recurrent neural pathways from cortical motor areas to the thalamus via basal ganglia and back to the cortex. Neuronal responses to internally and externally generated sequential movements have been studied in the motor and premotor cortex of monkeys, but the involvement of subcortical motor structures such as the thalamus have not been studied in monkeys or humans. We examined the activity of neurons during a sequential button press task in motor thalamus of parkinsonian as well as chronic pain patients undergoing implantation of deep brain stimulating electrodes. Single and dual microelectrode recordings were carried out during an internally generated task with a memorized sequence (MEM) and an externally driven task with the sequence given during task performance (follow). Average histograms of neuronal firing were constructed for each task and aligned with respect to visual cues (ready, go) or button presses (P1, P2, P3). Sequential movements were monitored with surface electromyography and hand accelerometry, and cell responses were divided into movement-defined epochs for ANOVA and post hoc means testing. Of 52 neurons tested, 31 were found to have task-related responses and 10 were task-selective with 4 responding preferentially to MEM and 7 responding preferentially to follow (1 was both). Complex responses were found including preparatory, delay period, and phase- and task-specific activity. These kinds of responses suggest a role of the thalamus in both internally and externally cued arms movement and provide some evidence for a role in sequential movements.     

Rhythmically firing neostriatal neurons in monkey: activity patterns during reaction-time hand movements.

While previous studies have identified rhythmically firing neurons (RFNs) in monkey neostriatum and these rhythmic firing patterns have been shown to evolve in neostriatal tonically active neurons (TANs) after dopamine input depletion, the activity patterns of RFNs during motor behavior are still far from completely understood. We examined the single-unit activity patterns of neostriatal neurons, recorded in awake behaving monkeys during a wrist movement task, for evidence of rhythmic activity. Monkeys made ballistic wrist flexion and extension movements in response to vibrotactile cues. Animals held a steady wrist position for 0.5 to 2.0 s while awaiting the onset of the go-cues (hold period). Although the majority of neostriatal neurons (274/306) did not fire rhythmically, approximately 10% of the neurons (32/306) fired rhythmically at 10-50 Hz during the hold period. Most RFNs (28/32) showed significant activity changes during the time between go-cue presentation and movement onset (premovement activity). One-half of RFNs exhibited premovement activity that differed as a function of movement direction. Only one RFN may have responded to the delivery of a fruit juice reward. Neuronal firing was analyzed using interspike interval distributions, autocorrelations, and serial correlation techniques. These analyses showed that the activity patterns of most RFNs were consistent with an integrate-and-fire model of neuronal rhythm generation. Changes in RFN activity patterns during the premovement interval and intertrial variations in firing frequency could be explained by changes in the general level of excitatory input. These observations are consistent with the firing properties reported for neostriatal cholinergic interneurons. It has been suggested that tonically active neurons may be cholinergic interneurons and that these neurons show changes in activity related to specific aspects of behavioral paradigms, such as rewards. RFNs may constitute a special class of TANs. The results presented here suggest that RFNs may have a role in movement initiation. We speculate that RFNs may modulate the propagation of cortical oscillations via basal ganglia-thalamic-cortical loops.     

Blink-perturbed saccades in monkey. II. Superior colliculus activity

Trigeminal reflex blinks evoked near the onset of a saccade cause profound spatial-temporal perturbations of the saccade that are typically compensated in mid-flight. This paper investigates the influence of reflex blinks on the discharge properties of saccade-related burst neurons (SRBNs) in intermediate and deep layers of the monkey superior colliculus (SC). Twenty-nine SRBNs, recorded in three monkeys, were tested in the blink-perturbation paradigm. We report that the air puff stimuli, used to elicit blinks, resulted in a short-latency ( approximately 10 ms) transient suppression of saccade-related SRBN activity. Shortly after this suppression (within 10-30 ms), all neurons resumed their activity, and their burst discharge then continued until the perturbed saccade ended near the extinguished target. This was found regardless whether the compensatory movement was into the cell's movement field or not. In the limited number of trials where no compensation occurred, the neurons typically stopped firing well before the end of the eye movement. Several aspects of the saccade-related activity could be further quantified for 25 SRBNs. It appeared that 1) the increase in duration of the high-frequency burst was well correlated with the (two- to threefold) increase in duration of the perturbed movement. 2) The number of spikes in the burst for control and perturbed saccades was quite similar. On average, the number of spikes increased only 14%, whereas the mean firing rate in the burst decreased by 52%. 3) An identical number of spikes were obtained between control and perturbed responses when burst and postsaccadic activity were both included in the spike count. 4) The decrease of the mean firing rate in the burst was well correlated with the decrease in the velocity of perturbed saccades. 5) Monotonic relations between instantaneous firing rate and dynamic motor error were obtained for control responses but not for perturbed responses. And 6) the high-frequency burst of SRBNs with short-lead and long-lead presaccadic activity (also referred to as burst and buildup neurons, respectively) showed very similar features. Our findings show that blinking interacts with the saccade premotor system already at the level of the SC. The data also indicate that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensation for blink-related perturbations. We propose that these interactions occur downstream from the motor SC and that the latter may encode the desired displacement vector of the eyes by sending an approximately fixed number of spikes to the brainstem saccadic burst generator.     

Single-unit activity in bulbar reticular formation during food ingestion in chronic cats

1. Single-unit activity was recorded from 215 neurons in the medial bulbar reticular formation during the masticatory sequence, from intake to deglutition, of 3 kinds of food (cat food pellets, canned fish, and milk) in 8 chronically prepared, unanesthetized, spontaneously respiring cats with their head fixed to a stereotaxic apparatus without pain or pressure. The firing patterns were compared to the simultaneously recorded EMGs of the jaw-closing and -opening muscles and to the jaw movement. 2. Fifty neurons changed their firing patterns during mastication. Nine neurons increased and one neuron decreased or stopped firing coincident with the masticatory sequence without an apparent rhythmical modulation of frequency corresponding with the masticatory rhythm (nonphasic group). The firing pattern of the remaining 40 neurons was modulated in phase with jaw movement (phasic group); 34 neurons either showed a spike burst or attained the highest firing frequency during the jaw-opening phase (opening type), while 6 neurons did so during the jaw-closing phase (closing type). The firing patterns of each neuron were essentially the same regardless of the kind of food ingested, except for 2 opening-type neurons that showed a rhythmical burst during mastication of solid food and tonic activity during lapping milk. 3. For 16 phasic neurons, there were significant correlations between some aspects of the firing pattern and a parameter of the movement during ingestion of solid food and/or milk. With one exception, these relationships did not appear to be due to sensory feedback. 4. We detected a monosynaptic excitatory projection from 3 opening-type neurons to the anterior digastric motoneurons, and monosynaptic inhibitory projections to the temporal or masseter motoneurons from 3 other opening-type neurons, by spike-triggered averaging of the full-wave rectified EMG of the jaw-closing and -opening muscles. No monosynaptic projections from the closing-type neurons or nonphasic group neurons to either jaw-opener or -closer motoneurons were detected. 5. The instantaneous firing frequency of all 3 inhibitor premotor neurons was positively correlated with the opening velocity, and the firing of 2 was also related to the jaw displacement.(ABSTRACT TRUNCATED AT 400 WORDS)     

Local nonspiking interneurons involved in gating of the descending motor pathway in crayfish

Uropod motor neurons in the terminal abdominal ganglion of crayfish are continuously excited during the abdominal posture movement so that subthreshold excitatory postsynaptic potentials from the descending statocyst pathway can elicit spike activity in the motor neurons only while the abdominal posture system is in operation. Local nonspiking interneurons in the terminal ganglion were also found to show sustained membrane potential change during the fictive abdominal posture movement. Artificial membrane potential change of these interneurons by intracellular current injection in the same direction as that actually observed during the abdominal movement caused similar excitation of uropod motor neurons. Artificial cancellation of the membrane potential change of these interneurons during the abdominal movement also caused cancellation of the excitation of uropod motor neurons. We concluded that the continuous excitation of uropod motor neurons during the fictive abdominal movement was mediated, at least partly, by the local nonspiking interneurons. Fourteen (36%) out of 39 examined nonspiking interneurons were judged to be involved in the excitation of uropod motor neurons during the fictive abdominal movement. Another 25 interneurons (64%) were found not to be involved in the excitation of motor neurons, although most of them had a strong effect on the uropod motor neuron activity when their membrane potential was changed artificially. The interneurons that were involved in the excitation of motor neurons during the abdominal movement included both of the two major structural types of nonspiking interneurons in the terminal ganglion, i.e., those in the anterolateral portion and those in the posterolateral portion. No strict correlation was found between the structure of nonspiking interneurons and their function in the control of uropod motor neuron activity.     

Influence of globus pallidus on arm movements in monkeys. I. Effects of kainic acid-induced lesions

The role of basal ganglia output via the globus pallidus (GP) was examined in monkeys trained to make rapid arm-reaching movements to a visual target in a reaction-time task. When neurons in the globus pallidus were destroyed by injection of kainic acid (KA) during task execution, contralateral arm movement times (MT) were increased significantly, with little or no change in reaction times (RT). The slowed movements were associated with a generalized depression in the amplitude and rate of rise of electromyographic (EMG) activity in all the contralateral muscles studied at the wrist, elbow, shoulder, and back, but there was no change in the sequential activation of these muscles. The most profound and persistent increases in movement time occurred when neurons were destroyed in the ventrolateral and caudal aspects of the internal as well as external pallidal segment. These results suggest a role for globus pallidus output in scaling the magnitude and/or buildup of EMG activity without affecting the initiation or the sequential organization of the programmed motor output.     

Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements.

1. Single-cell activity was recorded from three different motor areas in the cerebral cortex: the primary motor cortex (MI), supplementary motor area (SMA), and premotor cortex (PM). 2. Three monkeys (Macaca fuscata) were trained to perform a sequential motor task in two different conditions. In one condition (visually triggered task, VT), they reached to and touched three pads placed in a front panel by following lights illuminated individually from behind the pads. In the other condition (internally guided task, IT), they had to remember a predetermined sequence and press the three pads without visual guidance. In a transitional phase between the two conditions, the animals learned to memorize the correct sequence. Auditory instruction signals (tones of different frequencies) told the animal which mode it was in. After the instruction signals, the animals waited for a visual signal that triggered the first movement. 3. Neuronal activity was analyzed during three defined periods: delay period, premovement period, and movement period. Statistical comparisons were made to detect differences between the two behavioral modes with respect to the activity in each period. 4. Most, if not all, of MI neurons exhibited similar activity during the delay, premovement, and movement periods, regardless of whether the sequential motor task was visually guided or internally determined. 5. More than one-half of the SMA neurons were preferentially or exclusively active in relation to IT during both the premovement (55%) and movement (65%) periods. In contrast, PM neurons were more active (55% and 64% during the premovement and movement periods) in VT. 6. During the instructed-delay period, a majority of SMA neurons exhibited preferential or exclusive relation to IT whereas the activity in PM neurons was observed equally in different modes. 7. Two types of neurons exhibiting properties of special interest were observed. Sequence-specific neurons (active in a particular sequence only) were more common in SMA, whereas transition-specific neurons (active only at the transitional phase) were more common in PM. 8. Although a strict functional dichotomy is not acceptable, these observations support a hypothesis that the SMA is more related to IT, whereas PM is more involved in VT. 9. Some indications pointing to a functional subdivision of PM are obtained.     

The role of putamen and pallidum in motor initiation in the cat

The participation of basal ganglia in motor initiation was studied in six cats operantly trained to perform a ballistic flexion movement, triggered after a brief sound in a simple reaction time condition or delayed after the same sound in the presence of a tone cue. The activity of 356 neurons was recorded in the putamen and in the pallidum (globus pallidus and entopeduncular nucleus). A total of 19.4% of the neurons were not related to the conditioned flexion movement: they were either unrelated to the task (10.1%) or related to other periods of the motor performance such as trial beginning or reward delivery (9.3%). About 60% of the remaining neurons — defined as task-related — exhibited changes in firing rate that occurred, in the reaction time condition, less than 100 ms after the go signal and therefore began prior to movement onset. For most neurons, in the delayed condition, these early changes were absent, suggesting that their occurrence in the reaction time condition was not a sensory response but rather was related to the movement initiation. In addition, for many neurons these changes shifted in time, remaining time-locked to the movement. Correlations between these early changes in activity and motor parameters were demonstrated, suggesting that these changes were movement-related. For most neurons the firing levels observed during intertrial intervals and during foreperiod were similar. The mean discharge rate during the foreperiod was 19.2 impulses/s. Three patterns of activity were observed before movement: increases in discharge rate (61% of task-related neurons), transient decreases followed by increases (11%), or prolonged decreases (28%). Only minor differences were found between the characteristics of the populations of neurons recorded in the three sites under study: on average the neurons recorded in the globus pallidus were more active than the neurons recorded in the putamen or in the entopeduncular nucleus. The fact that, for certain neurons, the changes of activity prior to movement were different in reaction time condition and in delayed condition showed that the pattern of activity preceding movement might depend on the temporal requirements for motor initiation. Taken together with the motor effects obtained in the same task following GABA-receptor activation with muscimol microinjections in these structures, the present results suggest that putamen and pallidal neurons participate in the initiation of the conditioned movement under study.     

Segment interdependency and difficulty in two-stroke sequences

We previously demonstrated that velocity and movement time for the initial segment for a two-stroke movement are scaled in relation to the difficulty of the second segment. The interdependent kinematic changes were interpreted as evidence that movement planning/organization processes consider the movement parameters of both segments when determining the movement characteristics of the entire sequence. In this experiment we examined two-stroke movements where the difficulty of the first segment had either a low or high level of difficulty to determine if the interdependent kinematic changes are diminished when parameter specification is high for the initial segment. Two-stroke arm movements toward defined targets were made in the horizontal plane on an x-y digitizer. The direction of the first segment was an elbow extension movement away from the trunk. The direction of the second segment varied between forearm extension and flexion movements. Two different indexes of difficulty (IDs) of the first segment and two of the second segment were created by varying target size. In the low ID condition for the first segment, movement duration of the initial segment lengthened and peak velocity decreased when the ID of the second segment was increased, and this pattern was found for both the extension-extension and extension-flexion sequences. In contrast, when the level of difficulty was high for the first segment, the interdependencies disappeared for the extension-extension sequence: movement duration and peak velocity were unaffected by the difficulty of the second segment. For the extension-flexion sequence, however, the interdependencies were found in the movement time of the initial segment but were eliminated in the peak velocity, i.e., movement time increased, but the peak velocity did not change. Furthermore, for both the extension-extension and extension-flexion sequences, the intersegment interval was lengthened as the level of difficulty increased. These findings suggest that difficulty of the initial segment affects how the motor planning/organization processes treat adjacent segments of the sequence. In particular, the data support the hypothesis that when the initial movement segment has a high index of difficulty, motor planning/organization processes appear to treat the adjacent segments separately as two discrete actions.     

Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease

High-frequency stimulation (HFS) of the subthalamic nucleus (STN) or internal segment of the globus pallidus is a clinically successful treatment for the motor symptoms of Parkinson's disease. However, the mechanisms by which HFS alleviates these symptoms are not understood. Whereas initial studies focused on HFS-induced changes in neuronal firing rates, recent studies suggest that changes in patterns of neuronal activity may correlate with symptom alleviation. We hypothesized that effective STN HFS reduces the disorder of neuronal firing patterns in the basal ganglia thalamic circuit, minimizing the pathological activity associated with parkinsonism. Stimulating leads were implanted in the STN of two rhesus monkeys rendered parkinsonian by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Action potentials were recorded from neurons of the internal and external globus pallidus and the motor thalamus (ventralis anterior, ventralis lateralis pars oralis, and ventralis posterior lateralis pars oralis) during HFS that reduced motor symptoms and during clinically ineffective low-frequency stimulation (LFS). Firing pattern entropy was calculated from the recorded spike times to quantify the disorder of the neuronal activity. The firing pattern entropy of neurons within each region of the pallidum and motor thalamus decreased in response to HFS (n > or = 18 and P < or = 0.02 in each region), whereas firing rate changes were specific to pallidal neurons only. In response to LFS, firing rates were unchanged, but firing pattern entropy increased throughout the circuit (n > or = 24 and P < or = 10(-4) in each region). These data suggest that the clinical effectiveness of HFS is correlated with, and potentially mediated by, a regularization of the pattern of neuronal activity throughout the basal ganglia thalamic circuit.     

Trained slow tracking. II. Bidirectional discharge patterns of cerebellar nuclear, motor cortex, and spindle afferent neurons

Single-unit discharge was recorded in the dentate and interposed cerebellar nuclei, motor cortex, and C7 and C8 dorsal root ganglia during trained, slow hold-ramp-hold tracking, rapid alternating movement, torque-pulse perturbation, and action tremor of the monkey's wrist. Fifty-seven dentate and 45 interposed neurons were found in two monkeys that discharged in relation to slow tracking movement. Nearly all neurons had a distinct bidirectional pattern of discharge consisting of an abrupt increase (or decrease) in firing frequency at or before the onset of movement that was variably maintained throughout the ramp and was independent of movement direction. None of the neurons showed a clear relationship to direction, position, velocity, or load during the performance of this task. Nevertheless, many of these neurons discharged in relation to rapid alternation and (for interpositus) torque pulses in patterns that were directionally reciprocal. Some interpositus neurons showed a modulation related to tremor superimposed on the bidirectional discharge related to slow ramps. Twenty-nine neurons in motor cortex of one monkey discharged during slow hold-ramp-hold tracking in two patterns. Class I neurons (14 of 29) showed gradually changing, directionally reciprocal modulations of firing frequency for movements in opposite directions. These neurons were often related to torque load and/or to wrist position but not to velocity. The discharge pattern was similar to the pattern of activity of forearm muscles. Class II neurons (15 of 29) showed an abrupt change in firing frequency that was bidirectional. They were often related to torque load and/or to velocity but not to position. Motor cortex neurons discharged in relation to rapid alternating movements, torque pulses, and tremor in similar patterns that did not distinguish the two classes. Five units in dorsal root ganglia were identified as muscle spindle afferents. During ramps, their pattern of discharge was bidirectional and resembled the bidirectional discharge patterns of neurons in motor cortex (class II) and cerebellum. For some cells the bidirectional pattern varied slightly in relation to the direction and velocity of movement and the amount of torque load, but it was not related to the large changes in wrist position (muscle length). Modulation in relation to tremor was superimposed on the bidirectional pattern related to ramps. The comparison of spindle afferent discharge with the concurrent electromyogram (EMG) of the parent muscle suggested that spindles were driven by gamma-fusimotor activity dissociated from that of homonymous alpha-skeletomotor neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex

Neurophysiological recordings have revealed that the discharges of nearby cortical cells are positively correlated in time scales that range from millisecond synchronization of action potentials to much slower firing rate co-variations, evident in rates averaged over hundreds of milliseconds. The presence of correlated firing can offer insights into the patterns of connectivity between neurons; however, few models of population coding have taken account of the neuronal diversity present in cerebral cortex, notably a distinction between inhibitory and excitatory cells. We addressed this question in the monkey dorsolateral prefrontal cortex by recording neuronal activity from multiple micro-electrodes, typically spaced 0.2-0.3 mm apart. Putative excitatory and inhibitory neurons were distinguished based on their action potential waveform and baseline discharge rate. We tested each pair of simultaneously recorded neurons for presence of significant cross-correlation peaks and measured the correlation of their averaged firing rates in successive trials. When observed, cross-correlation peaks were centered at time 0, indicating synchronous firing consistent with two neurons receiving common input. Discharges in pairs of putative inhibitory interneurons were found to be significantly more strongly correlated than in pairs of putative excitatory cells. The degree of correlated firing was also higher for neurons with similar spatial receptive fields and neurons active in the same epochs of the behavioral task. These factors were important in predicting the strength of both short time scale (<5 ms) correlations and of trial-to-trial discharge rate covariations. Correlated firing was only marginally accounted for by motor and behavioral variations between trials. Our findings suggest that nearby inhibitory neurons are more tightly synchronized than excitatory ones and account for much of the correlated discharges commonly observed in undifferentiated cortical networks. In contrast, the discharge of pyramidal neurons, the sole projection cells of the cerebral cortex, appears largely independent, suggesting that correlated firing may be a property confined within local circuits and only to a lesser degree propagated to distant cortical areas and modules.     

Non-spatial,motor-specific activation in posterior parietal cortex

A localized cluster of neurons in macaque posterior parietal cortex, termed the parietal reach region (PRR), is activated when a reach is planned to a visible or remembered target. To explore the role of PRR in sensorimotor transformations, we tested whether cells would be activated when a reach is planned to an as-yet unspecified goal. Over one-third of PRR cells increased their firing after an instruction to prepare a reach, but not after an instruction to prepare a saccade, when the target of the movement remained unknown. A partially overlapping population (two-thirds of cells) was activated when the monkey was informed of the target location but not the type of movement to be made. Thus a subset of PRR neurons separately code spatial and effector-specific information, consistent with a role in specifying potential motor responses to particular targets.     

Fixation neurons in the superior colliculus encode distance between current and desired gaze positions

A visual scene is scrutinized during sequential periods of steady fixation, connected by saccades that shift the visual axis (gaze) to new positions. During such exploratory scan paths, gaze frequently strays from and then returns to salient features. How the brain keeps track of major end-goals and intermediate subgoals is not understood. We studied the discharge of fixation neurons of the brainstem's superior colliculus during multiple-step gaze shifts composed of a sequence of saccades made in the dark and separated by short periods of steady fixation. Cells were initially silent. As sequential gaze saccades approached the goal, firing began; its frequency increased progressively and peaked when gaze was on the remembered target location. We conclude that these fixation neurons encode the error between desired and actual gaze positions, irrespective of trajectory characteristics.