Effects of adaptation on orientation tuning in excitatory and inhibitory neurons in macaque V1 and V2

摘要

Adaptation modifies sensory pathways to adjust to the characteristics of the recently-encountered visual world. However, even for neuronal properties as fundamental as orientation, much is unknown about adaptation-induced alterations in tuning. To delineate the influence of adaptation on neural and network properties, we investigated its effect in functionally distinct cell categories (excitatory vs inhibitory) in two hierarchically-related brain regions, V1 and V2, of the primate visual pathway. We performed multitetrode recordings from 90 neurons in V1 and V2 of 6 macaques using drifting sinusoidal gratings, after adaptation to a preferred and a non-preferred orientation for brief (0.4 s) and prolonged (40 s) exposures. We found a wide range of tuning changes induced by adaptation. In layer 2/3, orientation selectivity either increased or decreased, and the tuning curve peak moved either towards (attractive) or away from (repulsive) the adapter. In contrast, Layer 4 neurons typically broadened their tuning after brief adaptation and narrowed their tuning after prolonged adaptation. In V1, findings were similar for inhibitory and excitatory neurons (as distinguished by their extracellular action potential shape). However, in V2, prolonged adaptation broadened the tuning of inhibitory cells, but narrowed the tuning of excitatory cells. Thus, there is a wide variety of tuning changes induced by adaptation in both V1 and V2, and dynamics of adaptation are distinct in excitatory and inhibitory neurons within V2. Notably, these findings have implications for the circuit mechanisms of orientation selectivity: attractive shifts do not occur in purely feedforward models, or in recurrent models in which inhibitory neurons are untuned. In sum, tuned inhibitory neurons contribute not only to orientation tuning, but also to how this tuning adapts a?? and hence, play a critical role in the neural representations that ultimately influence perception.