In macaque visual cortex, different cytochrome oxidase stripes of area V2 receive segregated projections from layers (L)2/3 and 4B of the
primary visual cortex (V1), and project to dorsal or ventral stream extrastriate areas. Parallel V1-to-V2 pathways suggest functionally
specialized circuits, but it is unknown whether these circuits arise from distinct cell types. V1 L4B includes two morphological types of
excitatory projection neurons: pyramids, which carry mixed magnocellular (M) and parvocellular (P) information to downstream areas,
and spiny stellates, which carry onlyMinformation. Previous studies have shown that, overall, V2 receives80% of its L4B inputs from
pyramids, thus receiving mixed M and P signals. However, it is unknown how pyramids and stellates distribute their outputs to the
different V2 stripes, and whether different stripes receive inputs from morphologically distinct neuron types. Using viral-mediated
labeling of V2-projecting L4B neurons in male macaques, we show that thick stripes receive a greater contribution of L4B inputs from
M-dominated spiny stellates compared with thin stripes. Both stripe types, however, receive a much larger contribution from spiny
stellates than previously shown for V2 overall, indicating that a larger amount ofMinformation than previously thought flows into both
the dorsal and ventral streams via the V2 thick and thin stripes, respectively. Moreover, we identify four types of V2-projecting L4B cells
differing in size and complexity. Three such cell types project to both thin and thick stripes, but one type, the giant spiny-stellate neuron,
resembling L4B neurons projecting to motion-sensitive area MT, was only found to project to thick stripes.
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Stream-specific feedback inputs to the primate primary visual cortex
The sensory neocortex consists of hierarchically-organized areas reciprocally connected via feedforward and feedback circuits. Feedforward connections shape the receptive field properties of neurons in higher areas within parallel streams specialized in processing specific stimulus attributes. Feedback connections have been implicated in top-down modulations, such as attention, prediction and sensory context. However, their computational role remains unknown, partly because we lack knowledge about rules of feedback connectivity to constrain models of feedback function. For example, it is unknown whether feedback connections maintain stream-specific segregation, or integrate information across parallel streams. Using viral-mediated labeling of feedback connections arising from specific cytochrome-oxidase stripes of macaque visual area V2, here we show that feedback to the primary visual cortex (V1) is organized into parallel streams resembling the reciprocal feedforward pathways. This suggests that functionally-specialized V2 feedback channels modulate V1 responses to specific stimulus attributes, an organizational principle potentially extending to feedback pathways in other sensory systems.
more » « less- Award ID(s):
- 1755431
- NSF-PAR ID:
- 10209428
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 12
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The cerebral cortex of primates encompasses multiple anatomically and physiologically distinct areas processing visual information. Areas V1, V2, and V5/MT are conserved across mammals and are central for visual behavior. To facilitate the generation of biologically accurate computational models of primate early visual processing, here we provide an overview of over 350 published studies of these three areas in the genus Macaca, whose visual system provides the closest model for human vision. The literature reports 14 anatomical connection types from the lateral geniculate nucleus of the thalamus to V1 having distinct layers of origin or termination, and 194 connection types between V1, V2, and V5, forming multiple parallel and interacting visual processing streams. Moreover, within V1, there are reports of 286 and 120 types of intrinsic excitatory and inhibitory connections, respectively. Physiologically, tuning of neuronal responses to 11 types of visual stimulus parameters has been consistently reported. Overall, the optimal spatial frequency (SF) of constituent neurons decreases with cortical hierarchy. Moreover, V5 neurons are distinct from neurons in other areas for their higher direction selectivity, higher contrast sensitivity, higher temporal frequency tuning, and wider SF bandwidth. We also discuss currently unavailable data that could be useful for biologically accurate models.
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It has been postulated that the brain is organized by “metamodal,” sensory-independent cortical modules capable of performing tasks (e.g., word recognition) in both “standard” and novel sensory modalities. Still, this theory has primarily been tested in sensory-deprived individuals, with mixed evidence in neurotypical subjects, thereby limiting its support as a general principle of brain organization. Critically, current theories of metamodal processing do not specify requirements for successful metamodal processing at the level of neural representations. Specification at this level may be particularly important in neurotypical individuals, where novel sensory modalities must interface with existing representations for the standard sense. Here we hypothesized that effective metamodal engagement of a cortical area requires congruence between stimulus representations in the standard and novel sensory modalities in that region. To test this, we first used fMRI to identify bilateral auditory speech representations. We then trained 20 human participants (12 female) to recognize vibrotactile versions of auditory words using one of two auditory-to-vibrotactile algorithms. The vocoded algorithm attempted to match the encoding scheme of auditory speech while the token-based algorithm did not. Crucially, using fMRI, we found that only in the vocoded group did trained-vibrotactile stimuli recruit speech representations in the superior temporal gyrus and lead to increased coupling between them and somatosensory areas. Our results advance our understanding of brain organization by providing new insight into unlocking the metamodal potential of the brain, thereby benefitting the design of novel sensory substitution devices that aim to tap into existing processing streams in the brain.
SIGNIFICANCE STATEMENT It has been proposed that the brain is organized by “metamodal,” sensory-independent modules specialized for performing certain tasks. This idea has inspired therapeutic applications, such as sensory substitution devices, for example, enabling blind individuals “to see” by transforming visual input into soundscapes. Yet, other studies have failed to demonstrate metamodal engagement. Here, we tested the hypothesis that metamodal engagement in neurotypical individuals requires matching the encoding schemes between stimuli from the novel and standard sensory modalities. We trained two groups of subjects to recognize words generated by one of two auditory-to-vibrotactile transformations. Critically, only vibrotactile stimuli that were matched to the neural encoding of auditory speech engaged auditory speech areas after training. This suggests that matching encoding schemes is critical to unlocking the brain's metamodal potential.
