Dept of Physiology, Anatomy and Genetics, Oxford University, Oxford, UK
Human visual perception of prolonged, static stimuli has been extensively investigated psychophysically, and yet the underlying neuronal activity remains largely unknown. Consider two simple examples. An image stabilised on the retina will be perceived to fade over the time course of several seconds. Conversely, following fixation of an image for several seconds, its removal will leave the subject with the perception of a negative afterimage. Along with a host of more elaborate visual aftereffects (including illusory figural, motion and contingent aftereffects), these phenomena can yield important clues to both the circuitry and functional activity at multiple stages of visual processing. However, a direct investigation of neuronal responses in this context is lacking.
We recorded extracellularly from the LGN and V1 in the anaesthetised, paralysed macaque, presenting both optimal sinusoidal gratings (”preferred”) and the opposite contrast gratings (”anti-preferred”) for varying amounts of time (1 to 64 s), followed by mean gray epochs.
In the LGN, P-cells showed a strong response which decayed exponentially (mean τ of ~20 s) to both onset of the preferred stimulus and the offset of the anti-preferred stimulus. Indeed, after repeated presentation of the anti-preferred grating over the course of several minutes, cells responded as strongly to the mean gray screen at stimulus offset as they had previously to the onset of the preferred stimulus. The build-up and decay of these after-responses was well fit by a simple exponentially adapting model. M-cells showed a different pattern of activity. In response to the preferred stimulus, they showed a strong response with both sustained and decaying components. However, the after-response at anti-preferred stimulus offset was always much less than the response to the preferred stimulus. We hypothesise the existence of an adapting element which is specific to the circuitry of the P-pathway.
In V1, we recorded the responses of orientation-tuned cells and found a strikingly different pattern of behaviour. Relative response amplitudes were somewhat scattered, with some cells responding more to the preferred stimulus, and others to the anti-preferred stimulus offset. However, after-response time constants were generally much shorter than those recorded in the LGN. The average response to anti-preferred stimulus offset decayed to baseline with τ of 1.3 s. Thus a second important question about visual pathway circuitry emerges: where and what is the gating mechanism which cuts short after-responses in V1 relative to the activity in LGN?
Support: the Wellcome Trust.