Effective connectivity of depth-structure-selective patches in the lateral bank of the macaque intraparietal sulcus

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.

纹外皮层区域（extrastriate cortical areas）通常由编码特定特征或刺激的神经元亚群组成，诸如颜色、视差或面部刺激；而编码相似刺激属性的神经元斑块，往往嵌入于相互连接的网络之中，例如注意网络或面部加工网络。本研究旨在探究同一皮层区域内，具备高度相似神经元响应特性的神经元亚区之间的有效连接。我们首先通过记录单单位与多单位神经活动，在猕猴顶内沟（intraparietal sulcus, IPS）前部定位了两个神经元斑块，二者均表现出相同的深度结构选择性；随后在功能磁共振成像（functional magnetic resonance imaging）扫描期间，对这两个斑块施加电微刺激，以明确二者的有效连接模式。我们所定位的这两个IPS亚区——虽具有相同的神经元响应特性，部分区域间距仅3毫米——在三只猕猴脑中，均与背侧和腹侧视觉通路上差异显著的皮层网络形成有效连接。反之，有效连接的差异，可解释前顶内沟内已知的视觉-运动梯度特性。上述结果阐明了前顶内沟作为关键脑区的功能角色：在物体分析过程中，背侧与腹侧视觉通路在此发生交互。因此，除皮层区域的解剖连接以及这些区域内单个神经元的响应特性外，有效连接为解析支持行为活动的广泛功能网络提供了全新的关键洞见。