Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS.

Extrastriate cortical areas are frequently composed of subpopulations of neurons encoding specific features or stimuli, such as color, disparity, or faces, and patches of neurons encoding similar stimulus properties are typically embedded in interconnected networks, such as the attention or face-processing network. The goal of the current study was to examine the effective connectivity of subsectors of neurons in the same cortical area with highly similar neuronal response properties. We first recorded single- and multi-unit activity to identify two neuronal patches in the anterior part of the macaque intraparietal sulcus (IPS) showing the same depth structure selectivity and then employed electrical microstimulation during functional magnetic resonance imaging in these patches to determine the effective connectivity of these patches. The two IPS subsectors we identified—with the same neuronal response properties and in some cases separated by only 3 mm—were effectively connected to remarkably distinct cortical networks in both dorsal and ventral stream in three macaques. Conversely, the differences in effective connectivity could account for the known visual-to-motor gradient within the anterior IPS. These results clarify the role of the anterior IPS as a pivotal brain region where dorsal and ventral visual stream interact during object analysis. Thus, in addition to the anatomical connectivity of cortical areas and the properties of individual neurons in these areas, the effective connectivity provides novel key insights into the widespread functional networks that support behavior.

Abstract■ Primates use vision to guide their actions in everyday life.

The exquisite ability of primates to grasp and manipulate objects relies on the transformation of visual information into motor commands. To this end, the visual system extracts object affordances that can be used to program and execute the appropriate grip. The macaque anterior intraparietal (AIP) area has been implicated in the extraction of affordances for the purpose of grasping. Neurons in the AIP area respond during visually guided grasping and to the visual presentation of objects. A subset of AIP neurons is also activated by two-dimensional images of objects and even by outline contours defining the object shape, but it is unknown how AIP neurons actually represent object shape. In this study, we used a stimulus reduction approach to determine the minimum effective shape feature evoking AIP responses. AIP neurons responding to outline shapes also responded selectively to very small fragment stimuli measuring only 1-2°. This fragment selectivity could not be explained by differences in eye movements or simple orientation selectivity, but proved to be highly dependent on the relative position of the stimulus in the receptive field. Our findings challenge the current understanding of the AIP area as a critical stage in the dorsal stream for the extraction of object affordances.

The primate visual system extracts object shape information for object recognition in the ventral visual stream. Recent research has demonstrated that object shape is also processed in the dorsal visual stream, which is specialized for spatial vision and the planning of actions. A number of studies have investigated the coding of 2D shape in the anterior intraparietal area (AIP), one of the end-stage areas of the dorsal stream which has been implicated in the extraction of affordances for the purpose of grasping. These findings challenge the current understanding of area AIP as a critical stage in the dorsal stream for the extraction of object affordances. The representation of three-dimensional (3D) shape has been studied in two interconnected areas known to be critical for object grasping: area AIP and area F5a in the ventral premotor cortex (PMv), to which AIP projects. In both areas neurons respond selectively to 3D shape defined by binocular disparity, but the latency of the neural selectivity is approximately 10 ms longer in F5a compared to AIP, consistent with its higher position in the hierarchy of cortical areas. Furthermore, F5a neurons were more sensitive to small amplitudes of 3D curvature and could detect subtle differences in 3D structure more reliably than AIP neurons. In both areas, 3D-shape selective neurons were co-localized with neurons showing motor-related activity during object grasping in the dark, indicating a close convergence of visual and motor information on the same clusters of neurons.