Abstract

Adaptation at early stages of sensory processing can be propagated to downstream areas. Such inherited adaptation is a potential confound for functional magnetic resonance imaging (fMRI) techniques that use selectivity of adaptation to infer neuronal selectivity. However, the relative contributions of inherited and intrinsic adaptation at higher cortical stages, and the impact of inherited adaptation on downstream processing, remain unclear. Using fMRI, we investigated how adaptation to visual motion direction and orientation influences visually evoked responses in human V1 and extrastriate visual areas. To dissociate inherited from intrinsic adaptation, we quantified the spatial specificity of adaptation for each visual area as a measure of the receptive field sizes of the area where adaptation originated, predicting that adaptation originating in V1 should be more spatially specific than adaptation intrinsic to extrastriate visual cortex. In most extrastriate visual areas, the spatial specificity of adaptation did not differ from that in V1, suggesting that adaptation originated in V1. Only in one extrastriate area—MT—was the spatial specificity of direction-selective adaptation significantly broader than in V1, consistent with a combination of inherited V1 adaptation and intrinsic MT adaptation. Moreover, inherited adaptation effects could be both facilitatory and suppressive. These results suggest that adaptation at early visual processing stages can have widespread and profound effects on responses in extrastriate visual areas, placing important constraints on the use of fMRI adaptation techniques, while also demonstrating a general experimental strategy for systematically dissociating inherited from intrinsic adaptation by fMRI.

Highlights

  • NEURAL ADAPTATION is a ubiquitous phenomenon that has been observed at multiple levels of the visual system, from the retina to extrastriate visual cortex (Kohn 2007; Solomon and Kohn 2014)

  • The effect of adaptation on the magnitude of event-related time courses shown in Fig. 2 was seen in the mean response amplitudes estimated for individual trials by a general linear model (GLM) fit (Fig. 3)

  • The results of the model fit were consistent with differences between V1 and MT spatial adaptation profiles being due to differences in Population adaptation field (pAF) size, but we considered whether differences in the contrast-response functions of V1 and MT could account for the observations

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Summary

Introduction

NEURAL ADAPTATION is a ubiquitous phenomenon that has been observed at multiple levels of the visual system, from the retina to extrastriate visual cortex (Kohn 2007; Solomon and Kohn 2014). Most research into adaptation mechanisms has focused on the properties of the neuronal populations undergoing adaptation, but there is growing recognition that adaptation effects can be propagated to downstream neuronal populations (Dhruv and Carandini 2014; Patterson et al 2014a, 2014b; Solomon et al 2004) Such “cascaded” or “inherited” adaptation complicates interpretation of the mechanisms, or functional role, of adaptation in several ways. In this study we have applied a variation of the methods used by Kohn and Movshon (2003) and Priebe et al (2002) to dissociate intrinsic and inherited fMRI adaptation effects for two basic visual stimulus features, motion and orientation. Several fMRI adaptation studies have found orientation-selective adaptation in multiple visual areas (e.g., Larsson et al 2006, 2010; Montaser-Kouhsari et al 2007), which could reflect multiple stages of adaptation or inherited adaptation effects or both

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