Decreases in neuronal activity and negative BOLD response in non-stimulated regions of monkey V1

Abstract

Background: 1. Numerous studies demonstrated that the response to a stimulus within the classical receptive field is modulated by an additional stimulus outside the receptive field. 2. A recent human fMRI study (Shmuel et al., Neuron 2002) demonstrated a robust sustained negative BOLD response (NBR) beyond the stimulated regions within retinotopic occipital areas. The NBR was associated with decreases in cerebral blood flow (CBF) and oxygen consumption, corroborating that the NBR could be triggered by decreases in neuronal activity. Aims: 1) Are there changes relative to spontaneous activity in non-stimulated regions in V1? 2) What are the neuronal correlates of the negative BOLD response? Methods: Monkeys were visually stimulated with iso-eccentricity rings of rotating checkers that subtended part of the visual-field (VF). A blank gray stimulus was used to measure the baseline cortical signal. Electrical recordings were obtained from the central VF representation in V1 simultaneously with fMRI. Results: Peripheral VF stimulus elicited positive/negative BOLD response in peripheral/more central VF representation in V1. The NBR was associated with decreases in neuronal activity (DsiNA), comparably large in action potentials, in the local-field potential and the multi-unit activity. DsiNA were observed up to 11 mm from the activated region in V1. The onsets of the increases and DsiNA were approximately concurrent, and the onset of the DsiNA preceded the corresponding onset of the NBR. Conclusions: 1) Non-stimulated regions adjacent to active regions in V1 decrease their neuronal activity. 2) The DsinNA cannot be exclusively mediated by the horizontal connections in V1. 3) The NBR in monkey V1 is associated with DsiNA that cannot be caused by hypoxia due to blood steal. 4) Most plausibly, the DsiNA trigger reductions in CBF that cause the NBR.

Footnotes

 Supported by the Max-Planck Society and a European Molecular Biology Organization long-term fellowship to AS.