Relationship between synchronous firing and multidimensional stimulus selectivity of neurons in macaque V1 and V4

概要

Visual information processing in the visual cortex is carried out in a hierarchical manner starting from the primary visual cortex (V1), and various features are extracted from the visual information of the external world. In addition, neurons in the visual cortex are functionally interconnected with neurons in the same or different cortical areas, and cooperative activity of these neurons represents visual information. Therefore, in order to understand hierarchical information processing in the visual cortex, it is important to compare the visual selectivity of single neurons and degree of synchronous firing among them in a common way, especially with respect to how pooling the output of neurons in upstream areas forms the visual response properties of neurons in a given area,

The degree of neural synchrony in the visual cortex was examined in previous studies with respect to similarity of orientation (OR) selectivity and/or physical distance. However, neurons in the visual cortex are selective not only for orientation, but also for other visual features. Especially the spatial frequency (SF) selectivity is important because both simple and complex cells in V1 exhibit it, and it is thought to contribute to the representation of visual information in the frequency domain as well as the OR selectivity. Here, I investigate whether the SF and OR selectivity of single neurons changes during visual information processing from V1 to V4, the intermediate stage of the ventral pathway. In addition, I also examine changes in the relationship between the similarity of multidimensional visual stimulus selectivity and the synchronous firing of neuron pairs within each area.

Penetrating the cortex with a 32-ch Michigan probe in presumed vertical direction, I recorded multiple single unit responses simultaneously in anesthetized and paralyzed macaque monkeys. These experiments were conducted separately on V1 and V4. Stimulus selectivity of each neuron was assessed via a reverse correlation technique by presenting a rapid succession of flashed gratings defined by OR, SF and spatial phase. The degree of synchronous firing, or strength of functional connectivity, between all pairs of neurons with visual stimulus selectivity was estimated by cross-correlation analysis.

Comparing the SF tuning of the V1 and V4 neurons, the optimal SF of the V4 neuron was lower than that of V1, and the SF bandwidth of the V4 neuron was wider than that of the V1 neuron. On the other hand, no such trend was observed for OR tuning. Furthermore, in the distribution of V4 neuron pairs with functional connectivity, there is a population of neuron pairs with large optimal OR differences (dOR) and a wide range of optimal SF ratios (rSF), unlike V1. Additionally, in contrast to V1, Within the mean response map area of V4 neurons, there is a significant relationship between the strength of functional connectivity and dOR of V4 neuron pairs with functional connectivity, but no significant relationship with rSF.

These results suggest that, while pooling in the SF dimension is implemented in visual information processing from V1 to V4, V4 neurons partially couple other neurons whose optimal ORs are far enough away from their own optimal ORs for various optimal SF ratios.