Unmasking Motion-Processing Activity in Human Brain Area V5/MT+ Mediated by Pathways That Bypass Primary Visual Cortex

Most models of the human visual system argue that higher-order motion-processing cortical regions receive their inputs only via the primary visual cortex (striate cortex), rather than also via direct projections from the thalamus that bypass primary visual cortex. However, recent evidence in non-human primates, along with some evidence in humans with damaged primary visual cortex (e.g., "blindsight" for motion in the blind visual hemifield), have argued for the existence of a direct thalamic-to-extrastriate projection for motion processing. This evidence remains controversial. Here we tested the idea that direct thalamic input to extrastriate motion processing areas exists in humans but might be masked in scalp recordings by activity from early visual areas. To do this, we employed stimuli that induced strong refractory effects in primary visual cortex--thereby creating a brief "reversable lesion" in primary visual cortex--immediately before the presentation of a motion stimulus. Under these conditions, we then assessed whether motion areas of cortex were still able to process the motion stimuli by recording event-related potentials (ERPs) and event-related magnetic fields (ERFs/MEG). We found robust motion-related activity in extrastriate motion processing areas in the ERP and MEG signals even when primary visual cortex was heavily suppressed by our manipulation. This finding provides evidence for a direct thalamic functional pathway to extrastriate visual cortical motion processing areas in the human that bypasses primary visual cortex.

[1]  S Zeki,et al.  Conscious visual perception without V1. , 1993, Brain : a journal of neurology.

[2]  C Blakemore,et al.  Direction discrimination of moving gratings and plaids and coherence in dot displays without primary visual cortex (V1) , 1998, The European journal of neuroscience.

[3]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  C. Gross Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex , 1991, Neuropsychologia.

[5]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R J Ilmoniemi,et al.  Transcranial magnetic stimulation--a new tool for functional imaging of the brain. , 1999, Critical reviews in biomedical engineering.

[7]  S. Zeki,et al.  The consequences of inactivating areas V1 and V5 on visual motion perception. , 1995, Brain : a journal of neurology.

[8]  L. Benevento,et al.  The organization of connections between the pulvinar and visual area MT in the macaque monkey , 1983, Brain Research.

[9]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  C. N. Guy,et al.  The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex. , 1995, Brain : a journal of neurology.

[11]  M. Yukie,et al.  Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys , 1981, The Journal of comparative neurology.

[12]  W. Fries The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[14]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  S. Shimojo,et al.  Manifestation of scotomas created by transcranial magnetic stimulation of human visual cortex , 1999, Nature Neuroscience.

[16]  S. Zeki,et al.  The Riddoch syndrome: insights into the neurobiology of conscious vision. , 1998, Brain : a journal of neurology.

[17]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[18]  Karl Zilles,et al.  Architecture, Connectivity, and Transmitter Receptors of Human Extrastriate Visual Cortex , 1997 .