Mapping Horizontal Spread of Activity in Monkey Motor Cortex Using Single Pulse Microstimulation

Abstract

Anatomical studies have demonstrated that distant cortical points are interconnected through long range axon collaterals of pyramidal cells. However, the functional properties of these intrinsic synaptic connections, especially their relationship with the cortical representations of body movements, have not been systematically investigated. To address this issue, we used multielectrode arrays chronically implanted in the motor cortex of two rhesus monkeys to analyze the effects of single-pulse intracortical microstimulation (sICMS) applied at one electrode on the neuronal activities recorded at all other electrodes. The temporal and spatial distribution of the evoked responses of single and multiunit activities was quantified to determine the properties of horizontal propagation. The typical responses were characterized by a brief excitatory peak followed by inhibition of longer duration. Significant excitatory responses to sICMS could be evoked up to 4 mm away from the stimulation site, but the strength of the response decreased exponentially and its latency increased linearly with the distance. We then quantified the direction and strength of the propagation in relation to the somatotopic organization of the motor cortex. We observed that following sICMS the propagation of neural activity is mainly directed rostro-caudally near the central sulcus but follows medio-lateral direction at the most anterior electrodes. The fact that these interactions are not entirely symmetrical may characterize a critical functional property of the motor cortex for the control of upper limb movements. Overall, these results support the assumption that the motor cortex is not functionally homogeneous but forms a complex network of interacting subregions.

In vitro characterization of intrinsic properties and local synaptic inputs to pyramidal neurons in macaque primary motor cortex

“…Our recordings were made at only single points, relatively close to the stimulation array. It is known that M1 cells can be activated transynaptically by stimuli delivered several millimetres away (Baker et al., ; Hao, Riehle, & Brochier, ). This is the case for identified pyramidal tract cells, which are located in layer V, when stimuli are also given to layer V (Baker et al., ).…”

Synchronization, stochasticity and phase waves in neuronal networks with spatially-structured connectivity

“…The underlying assumption in Eq. (16) is that the phase difference plays a dominant role in the difference of activities between the two E-I modules because the phase difference mode has a much smaller restoring strength than the other (amplitude) mode between the two modules. The respective eigenvalues of the two modes are shown in Fig.…”

“…For very small coupling strengths, the phase approximation with the full limit cycle dynamics (Eqs. (16,82), dotted lines) gives a good account of the observed synchronization, while for larger couplings both phase and amplitude modulations have to be considered (two-mode calculation, Eq. (97), solid black line).…”

“…These waves appear to propagate along particular anatomical directions with a typical wavelength of 1 cm and a velocity of about 20 cm · s −1 [10]. On the structural side, the characterization of the long-range intracortical connectivity in motor cortex have given rise to several quantification endeavors in both monkeys [15,16] and cats [17] with the strength of excitatory responses to microstimulation decaying on a 2 mm length scale. Can one connect these different observations in some ways and how?…”

Propagating patterns of activity across motor cortex facilitate movement initiation

“…Retrograde axon degeneration following punctate lesions in M1 has indicated longer range horizontal connectivity along the rostro-caudal axis as compared to the medial-lateral axis 42 . Moreover, an ICMS study has provided evidence for dominant functional connectivity along the rostro-caudal axis 43 .…”