Circuits for Local and Global Signal Integration in Primary Visual Cortex

Abstract

Contrast-dependent changes in spatial summation and contextual modulation of primary visual cortex (V1) neuron responses to stimulation of their receptive field reveal long-distance integration of visual signals within V1, well beyond the classical receptive field (cRF) of single neurons. To identify the cortical circuits mediating these long-distance computations, we have used a combination of anatomical and physiological recording methods to determine the spatial scale and retinotopic logic of intra-areal V1 horizontal connections and inter-areal feedback connections to V1. We have then compared the spatial scales of these connectional systems to the spatial dimensions of the cRF, spatial summation field (SF), and modulatory surround field of macaque V1 neurons. We find that monosynaptic horizontal connections within area V1 are of an appropriate spatial scale to mediate interactions within the SF of V1 neurons and to underlie contrast-dependent changes in SF size. Contrary to common beliefs, these connections cannot fully account for the dimensions of the surround field. The spatial scale of feedback circuits from extrastriate cortex to V1 is, instead, commensurate with the full spatial range of center-surround interactions. Thus these connections could represent an anatomical substrate for contextual modulation and global-to-local integration of visual signals. Feedback projections connect corresponding and equal-sized regions of the visual field in striate and extrastriate cortices and cover anisotropic parts of visual space, unlike V1 horizontal connections that are isotropic in the macaque. V1 isotropic connectivity demonstrates that anisotropic horizontal connections are not necessary to generate orientation selectivity. Anisotropic feedback connections may play a role in contour completion.

Intact Spectral but Abnormal Temporal Processing of Auditory Stimuli in Autism

“…Perception of complex patterns on the other hand requires communication among multiple cortical regions, which, in case of reduced functional synchrony, would operate less efficient. In visual perception, feedforward (from V1 to V2-V4) and feedbackward connections that amplify activity of neurons in J Autism Dev Disord (2009) 39:742-750 747 lower order areas (from V2-V4 to V1) are needed to perceive complex patterns (Angelucci et al 2002). Likewise, in the auditory system, communication between A1 and A2, and furthermore, feedforward and feedback communication between the auditory cortex and subcortical nuclei such as the inferior colliculus are needed for the perception of spectro-temporally complex sounds and their segregation from background noise (Khalfa et al 2001a).…”

Occipital network for figure/ground organization

“…Is the link between V1/V2 and hMT+ a plausible mechanism for contextual inXuence in general? Anatomically, both feedforward and feedback connections between V1/V2 and MT are well-established by retrograde tracer techniques (Tigges et al 1981;Maunsell and van Essen 1983;Ungerleider and Desimone 1986;Krubitzer and Kaas 1990;Rockland and Van Hoesen 1994;Angelucci et al 2002). MT is one of the primary output pathways for layer six neurons of these early retinotopic regions (Rockland and Van Hoesen 1994;Rockland and Knutson 2000).…”

Learning and inference in the brain

“…Forwards connections (from a low to a high level) have sparse axonal bifurcations and are topographically organised, originating in supragranular layers and terminating largely in layer IV. Backward connections, on the other hand, show abundant axonal bifurcation and a more diffuse topography, although they can be patchy (Angelucci et al, 2002b). Their origins are bilaminar/infragranular and they terminate predominantly in supragranular layers (Rockland & Pandya, 1979;Salin & Bullier, 1995).…”