Primary sensorimotor cortex exhibits complex dependencies of spike-field coherence on neuronal firing rates, field power, and behavior.

Spike-field coherence (SFC) is widely used to assess cortico-cortical interactions during sensorimotor behavioral tasks by measuring the consistency of the relative phases between the spike train of a neuron and the concurrent local field potentials (LFPs). Interpretations of SFC as a measure of functional connectivity are complicated by theoretical work suggesting that estimates of SFC depend on overall neuronal activity. We evaluated the dependence of SFC on neuronal firing rates, LFP power, and behavior in the primary motor (MIo) and primary somatosensory (SIo) areas of the orofacial sensorimotor cortex of monkeys ( Macaca mulatta) during performance of a tongue-protrusion task. Although we occasionally observed monotonically increasing linear relationships between coherence and firing rate, we most often found highly complex, nonmonotonic relationships in both SIo and MIo and sometimes even found that coherence decreased with increasing firing rate. The lack of linear relationships was also true for both LFP power and tongue-protrusive force. Moreover, the ratio between maximal firing rate and the firing rate at peak coherence deviated significantly from unity, indicating that MIo and SIo neurons achieved maximal SFC at a submaximal level of spiking. Overall, these results point to complex relationships of SFC to firing rates, LFP power, and behavior during sensorimotor cortico-cortical interactions: coherence is a measure of functional connectivity whose magnitude is not a mere monotonic reflection of changes in firing rate, LFP power, or the relevantly controlled behavioral parameter. NEW & NOTEWORTHY The concern that estimates of spike-field coherence depend on the firing rates of single neurons has influenced analytical methods employed by experimental studies investigating the functional interactions between cortical areas. Our study shows that the overwhelming majority of the estimated spike-field coherence exhibited complex relations with firing rates of neurons in the orofacial sensorimotor cortex. The lack of monotonic relations was also evident after testing the influence of local field potential power and force on spike-field coherence.

Directional information from neuronal ensembles in the primate orofacial sensorimotor cortex.

Neurons in the arm and orofacial regions of the sensorimotor cortex in behaving monkeys display directional tuning of their activity during arm reaching and tongue protrusion, respectively. While studies on population activity abound for the arm motor cortex, how populations of neurons from the orofacial sensorimotor cortex represent direction has never been described. We therefore examined and compared the directional information contained in the spiking activity of populations of single neurons recorded simultaneously from chronically implanted microelectrode arrays in the orofacial primary motor (MIo, N = 345) and somatosensory (SIo, N = 336) cortices of monkeys (Macaca mulatta) as they protruded their tongue in different directions. Differential modulation to the direction of tongue protrusion was found in >60% of task-modulated neurons in MIo and SIo and was stronger in SIo (P < 0.05). Moreover, mutual information between direction and spiking was significantly higher in SIo compared with MIo at force onset and force offset (P < 0.01). Finally, the direction of tongue protrusion was accurately predicted on a trial-by-trial basis from the spiking activity of populations of MIo or SIo neurons by using a discrete decoder (P < 0.01). The highly reliable decoding was comparable between MIo and SIo neurons. However, the temporal evolution of the decoding performance differed between these two areas: MIo showed late-onset, fast-rising, and phasic performance, whereas SIo exhibited early-onset, slow-rising, and sustained performance. Overall, the results suggest that both MIo and SIo are highly involved in representing the direction of tongue protrusion but they differ in the amplitude and temporal processing of the directional information distributed across populations of neurons.

Behavioral demonstration of a somatosensory neuroprosthesis.

Tactile sensation is critical for effective object manipulation, but current prosthetic upper limbs make no provision for delivering somesthetic feedback to the user. For individuals who require use of prosthetic limbs, this lack of feedback transforms a mundane task into one that requires extreme concentration and effort. Although vibrotactile motors and sensory substitution devices can be used to convey gross sensations, a direct neural interface is required to provide detailed and intuitive sensory feedback. In light of this, we describe the implementation of a somatosensory prosthesis with which we elicit, through intracortical microstimulation (ICMS), percepts whose magnitude is graded according to the force exerted on the prosthetic finger. Specifically, the prosthesis consists of a sensorized finger, the force output of which is converted into a regime of ICMS delivered to primary somatosensory cortex through chronically implanted multi-electrode arrays. We show that the performance of animals (Rhesus macaques) on a tactile task is equivalent whether stimuli are delivered to the native finger or to the prosthetic finger.

Excess synchrony in motor cortical neurons provides redundant direction information with that from coarse temporal measures.

Previous studies have shown that measures of fine temporal correlation, such as synchronous spikes, across responses of motor cortical neurons carries more directional information than that predicted from statistically independent neurons. It is also known, however, that the coarse temporal measures of responses, such as spike count, are not independent. We therefore examined whether the information carried by coincident firing was related to that of coarsely defined spike counts and their correlation. Synchronous spikes were counted in the responses from 94 pairs of simultaneously recorded neurons in primary motor cortex (MI) while monkeys performed arm movement tasks. Direct measurement of the movement-related information indicated that the coincident spikes (1- to 5-ms precision) carry approximately 10% of the information carried by a code of the two spike counts. Inclusion of the numbers of synchronous spikes did not add information to that available from the spike counts and their coarse temporal correlation. To assess the significance of the numbers of coincident spikes, we extended the stochastic spike count matched (SCM) model to include correlations between spike counts of the individual neural responses and slow temporal dependencies within neural responses (approximately 30 Hz bandwidth). The extended SCM model underestimated the numbers of synchronous spikes. Therefore as with previous studies, we found that there were more synchronous spikes in the neural data than could be accounted for by this stochastic model. However, the SCM model accounts for most (R(2) = 0.93 +/- 0.05, mean +/- SE) of the differences in the observed number of synchronous spikes to different directions of arm movement, indicating that synchronous spiking is directly related to spike counts and their broad correlation. Further, this model supports the information theoretic analysis that the synchronous spikes do not provide directional information beyond that available from the firing rates of the same pool of directionally tuned MI neurons. These results show that detection of precisely timed spike patterns above chance levels does not imply that those spike patterns carry information unavailable from coarser population codes but leaves open the possibility that excess synchrony carries other forms of information or serves other roles in cortical information processing not studied here.

Neuronal interactions improve cortical population coding of movement direction.

Interactions among groups of neurons in primary motor cortex (MI) may convey information about motor behavior. We investigated the information carried by interactions in MI of macaque monkeys using a novel multielectrode array to record simultaneously from 12-16 neurons during an arm-reaching task. Pairs of simultaneously recorded cells revealed significant correlations in their trial-to-trial firing rate variation when estimated over broad (600 msec) time intervals. This covariation was only weakly related to the preferred directions of the individual MI neurons estimated from the firing rate and did not vary significantly with interelectrode distance. Most significantly, in a portion of cell pairs, correlation strength varied with the direction of the arm movement. We evaluated to what extent correlated activity provided additional information about movement direction beyond that available in single neuron firing rate. A multivariate statistical model successfully classified direction from single trials of neural data. However, classification was consistently better when correlations were incorporated into the model as compared to one in which neurons were treated as independent encoders. Information-theoretic analysis demonstrated that interactions caused by correlated activity carry additional information about movement direction beyond that based on the firing rates of independently acting neurons. These results also show that cortical representations incorporating higher order features of population activity would be richer than codes based solely on firing rate, if such information can exploited by the nervous system.

Information about movement direction obtained from synchronous activity of motor cortical neurons.

Although neuronal synchronization has been shown to exist in primary motor cortex (MI), very little is known about its possible contribution to coding of movement. By using cross-correlation techniques from multi-neuron recordings in MI, we observed that activity of neurons commonly synchronized around the time of movement initiation. For some cell pairs, synchrony varied with direction in a manner not readily predicted by the firing of either neuron. Information theoretic analysis demonstrated quantitatively that synchrony provides information about movement direction beyond that expected by simple rate changes. Thus, MI neurons are not simply independent encoders of movement parameters but rather engage in mutual interactions that could potentially provide an additional coding dimension in cortex.

Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements.

The role of "fast," or gamma band (20-80 Hz), local field potential (LFP) oscillations in representing neuronal activity and in encoding motor behavior was examined in motor cortex of two alert monkeys. Using chronically implanted microwires, we simultaneously recorded LFPs and single or multiple unit (MU) discharge at a group of sites in the precentral gyrus during trained finger force or reaching movements, during natural reaching and grasping, and during quiet sitting. We evaluated the coupling of oscillations with task-related firing at the same site, the timing of oscillations with respect to the execution of trained and untrained movement, and the temporal synchrony of oscillations across motor cortical sites. LFPs and neural discharge were examined from a total of 16 arm sites (7 sites in 1 monkey and 9 in the other), each showing movement-related discharge modulation and arm microstimulation effects. In the trained tasks, fast LFP and MU oscillations occurred most often during a premovement delay period, ceasing around movement onset. The decrease in oscillation roughly coincided with the appearance of firing rate modulation coupled to the motor action. During this delay, LFP oscillations exhibited either "overlapping" or "mixed" relationships with the simultaneously recorded neural discharge at that site. Overlap was characterized by coincident epochs of increased neural discharge and LFP oscillations. For the mixed pattern, episodes of LFP oscillation typically coincided with periods of diminished firing but overlap also sometimes appeared. Both patterns occurred concurrently across motor cortex during preparation; LFP suppression with motor action was ubiquitous. Fast oscillations reappeared quickly upon transition from quiet sitting to resumption of task performance, indicating an association with task engagement, rather than the general motor inaction of the delay period. In contrast to trained movements, fast oscillations often appeared along with movement during untrained reaching, but oscillations occurred erratically and were not reliably correlated with elevated neural discharge. Synchronous oscillations occurred at sites as much as 5 mm apart, suggesting widespread coupling of neurons and LFP signals in motor cortex. Widespread coupling of oscillatory signals is consistent with the concept that temporal coding processes operate in motor cortex. However, because the relationship between neuronal discharge and the appearance of fast oscillations may be altered by behavioral condition, they must reflect a global process active in conjunction with motor planning or preparatory functions, but not details of motor action encoded in neuronal firing rate.

Coupling the neural and physical dynamics in rhythmic movements.

A pair of coupled oscillators simulating a central pattern generator (CPG) interacting with a pendular limb were numerically integrated. The CPG was represented as a van der Pol oscillator and the pendular limb was modeled as a linearized, hybrid spring-pendulum system. The CPG oscillator drove the pendular limb while the pendular limb modulated the frequency of the CPG. Three results were observed. First, sensory feedback influenced the oscillation frequency of the coupled system. The oscillation frequency was lower in the absence of sensory feedback. Moreover, if the muscle gain was decreased, thereby decreasing the oscillation amplitude of the pendular limb and indirectly lowering the effect of sensory feedback, the oscillation frequency decreased monotonically. This is consistent with experimental data (Williamson and Roberts 1986). Second, the CPG output usually led the angular displacement of the pendular limb by a phase of 90 degrees regardless of the length of the limb. Third, the frequency of the coupled system tuned itself to the resonant frequency of the pendular limb. Also, the frequency of the coupled system was highly resistant to changes in the endogenous frequency of the CPG. The results of these simulations support the view that motor behavior emerges from the interaction of the neural dynamics of the nervous system and the physical dynamics of the periphery.

Resonance Tuning in Rhythmic Arm Movements.

The hypothesis was tested that the preferred frequency of rhythmic movement corresponds to the resonant frequency of the muscle-limb system, as proposed by the hybrid spring-pendulum model (Kugler Turvey, 1987). In contrast to previous studies, the resonant frequency and stiffness of the system were estimated independently, which permitted quantitative predictions of the preferred frequency to be made. Human subjects (N = 5) were asked to oscillate their forearms in the vertical plane at their preferred frequency under conditions of added mass and external spring loading. Subjects also oscillated their arms at frequencies below and above the preferred frequency, which enabled the investigators to estimate the resonant frequency and stiffness of the elbow joint by using the phase transfer method (Viviani, Soechting, Terzuolo, 1976). The preferred frequency corresponded to the resonant frequency of the muscle-limb system under each condition, as predicted. The oscillation amplitude varied inversely with the preferred frequency, which was also predicted. Finally, the internal joint stiffness was modulated so that it matched the impedance of the external springs but was unaffected by added mass. The results are consistent with an autonomous oscillator model that incorporates proprioception about the dynamics of the periphery.

Hysteresis reduction in proprioception using presynaptic shunting inhibition.

1. The tonic responses of angular-position-sensitive afferents in the metathoracic chordotonal organ of the locust leg exhibit much hysteresis. For a given joint angle, the ratio of an afferent's tonic firing rate after extension to its firing rate after flexion (or vice versa) is typically between 1.2:1 and 3:1 but can be as large as 10:1. Spiking local interneurons, that receive direct inputs from these afferents, can, by contrast, exhibit much less hysteresis (between 1.1:1 and 1.2:1). We tested the hypothesis that presynaptic inhibitory interactions between afferent axons reduces the hysteresis of postsynaptic interneurons by acting as an automatic gain control mechanism. 2. We used two kinds of neural models to test this hypothesis: 1) an abstract nonspiking neural model in which a multiplicative, shunting term reduced the "firing rate" of the afferent and 2) a more realistic compartmental model in which shunting inhibition presynaptically attenuated the amplitude of the action potentials reaching the afferent terminals. 3. The abstract neural model demonstrated the automatic gain control capability of a network of laterally inhibited afferent units. A postsynaptic unit, which was connected to the competitive network of afferents, coded for joint angle without saturating as the strength of the afferent input increased by two orders of magnitude. This was possible because shunting inhibition exactly balanced the increase in the excitatory input. This compensatory mechanism required the sum of the excitatory and inhibitory conductances to be much larger than the leak conductance. This requirement suggested a graded weighting scheme in which the afferent recruited first (i.e., at a small joint angle) received the largest inhibition from each of the other afferents because of the lack of active neighbors, and the afferent recruited last (i.e., at a large joint angle) received the least inhibition because all the other afferents were active. 4. The compartmental model demonstrated that presynaptic shunting inhibition between afferents could decrease the average synaptic conductance caused by the afferents onto the spiking interneuron, thereby counterbalancing the afferents' large average firing rates after movements in the preferred direction. Therefore the total postsynaptic input per unit time did not differ much between the preferred and nonpreferred directions.(ABSTRACT TRUNCATED AT 400 WORDS)

Is a virtual trajectory necessary in reaching movements?

The mass-spring model of limb control was extended to two-joint arm movements in the horizontal plane and tested against kinematic data from human subjects. Two versions of the model were compared in order to test the idea that the equilibrium position of the hand moves along a "virtual" trajectory as demonstrated in single-joint arm movements (Bizzi et al. 1982, 1984; Latash and Gottlieb 1991). In the peripheral version, the equilibrium position was shifted abruptly, while the torques generated at the joints are gated by rise-time functions. In the central version, the equilibrium position was updated gradually according to a predefined trajectory. The paths and tangential velocity profiles of the hand generated by these two versions were compared to Morasso's (1981) experimental data. The central version generally performed better throughout the workspace except in certain special directions. Moreover, its paths exhibited more stability as the movement speed was varied.

On the sufficiency of the velocity field for perception of heading.

All models of self-motion from optical flow assume the instantaneous velocity field as input. We tested this assumption for human observers using random-dot displays that simulated translational and circular paths of movement by manipulating the lifetime and displacement of individual dots. For translational movement, observers were equally accurate in judging direction of heading from a "velocity field" with a two-frame dot life and a "direction field" in which the magnitudes of displacement were randomized while the radial pattern of directions was preserved, but at chance with a "speed field" in which the directions were randomized, preserving only magnitude. Accuracy declined with increasing noise in vector directions, but remained below 2.6 degrees with a 90 degrees noise envelope. Thus, the visual system uses the radial morphology of vector directions to determine translational heading and can tolerate large amounts of noise in this pattern. For circular movement, observers were equally accurate with a 2-frame "velocity field", 3-frame "acceleration" displays, and 2-frame and 3-frame "direction fields", consistent with the use of the pattern of vector directions to locate the center of rotation. The results indicate that successive independent velocity fields are sufficient for perception of translational and circular heading.