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Hierarchical stimulus processing in rodent primary and lateral visual cortex as assessed through neuronal selectivity and repetition suppression.

ABSTRACT: Similar to primates, visual cortex in rodents appears to be organized in two distinct hierarchical streams. However, there is still little known about how visual information is processed along those streams in rodents. In this study, we examined how repetition suppression and position and clutter tolerance of the neuronal representations evolve along the putative ventral visual stream in rats. To address this question, we recorded multiunit spiking activity in primary visual cortex (V1) and the more downstream visual laterointermediate (LI) area of head-restrained Long-Evans rats. We employed a paradigm reminiscent of the continuous carry-over design used in human neuroimaging. In both areas, stimulus repetition attenuated the early phase of the neuronal response to the repeated stimulus, with this response suppression being greater in area LI. Furthermore, stimulus preferences were more similar across positions (position tolerance) in area LI than in V1, even though the absolute responses in both areas were very sensitive to changes in position. In contrast, the neuronal representations in both areas were equally good at tolerating the presence of limited visual clutter, as modeled by the presentation of a single flank stimulus. When probing tolerance of the neuronal representations with stimulus-specific adaptation, we detected no position tolerance in either examined brain area, whereas, on the contrary, we revealed clutter tolerance in both areas. Overall, our data demonstrate similarities and discrepancies in processing of visual information along the ventral visual stream of rodents and primates. Moreover, our results stress caution in using neuronal adaptation to probe tolerance of the neuronal representations. NEW & NOTEWORTHY Rodents are emerging as a popular animal model that complement primates for studying higher level visual functions. Similar to findings in primates, we demonstrate a greater repetition suppression and position tolerance of the neuronal representations in the downstream laterointermediate area of Long-Evans rats compared with primary visual cortex. However, we report no difference in the degree of clutter tolerance between the areas. These findings provide additional evidence for hierarchical processing of visual stimuli in rodents.

SUBMITTER: Kaliukhovich DA

PROVIDER: S-EPMC6171059 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Hierarchical stimulus processing in rodent primary and lateral visual cortex as assessed through neuronal selectivity and repetition suppression.

Kaliukhovich Dzmitry A DA Op de Beeck Hans H

Journal of neurophysiology 20180509 3

Similar to primates, visual cortex in rodents appears to be organized in two distinct hierarchical streams. However, there is still little known about how visual information is processed along those streams in rodents. In this study, we examined how repetition suppression and position and clutter tolerance of the neuronal representations evolve along the putative ventral visual stream in rats. To address this question, we recorded multiunit spiking activity in primary visual cortex (V1) and the ...[more]

PMID: 29742022

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Project description:Sensory experience is necessary for the development of some receptive field properties of neurons in primary sensory cortical areas. However, it remains unclear whether the parameters of an individual animal's experience play an instructive role and influence the tuning parameters of cortical sensory neurons as selectivity emerges, or rather whether experience merely permits the completion of processes that are fully seeded at the onset of experience. Here we have examined whether the speed of visual stimuli that are presented to visually naive ferrets can influence the parameters of speed tuning and direction selectivity in cortical neurons. Visual experience is necessary for the development of direction selectivity in carnivores. If, during development, cortical neurons had the flexibility to choose from among different inputs with a range of spatial positions and temporal delays, then correlation-based plasticity mechanisms could instruct the precise spatiotemporal selectivity that underlies speed tuning and direction selectivity, and the parameters of an individual animal's experience would influence the tuning that emerges. Alternatively, the tuning parameters of these neurons may already be established at the onset of visual experience, and experience may merely permit the expression of this tuning. We found that providing different groups of animals with either slow (12.5 deg/s) or fast (50 deg/s) visual stimuli resulted in emergence of direction selectivity, but that speed tuning and direction selectivity were similar in the two groups. These results are more consistent with a permissive role for experience in the development of direction selectivity.SIGNIFICANCE STATEMENT The proper development of brain circuits and neural response properties depends on both nature (factors independent of experience) and nurture (factors dependent on experience). In this study, we examined whether the quality of visual experience of an individual animal influences the development of basic sensory detectors in primary visual cortex. We found that, although visual experience is required for the development of direction selectivity, tuning for stimulus speed could not be altered by specific experience with slow or fast stimuli. These results suggest that the tuning parameters for direction selectivity are specified independently of an animal's sensory experience, and that a range of experiences can promote the proper mature expression of direction selectivity in primary visual cortex.

Project description:Neurons in the mouse primary visual cortex (V1) exhibit characteristic response selectivity to visual stimuli, such as orientation, direction and spatial frequency selectivity. Since V1 receives thalamic visual inputs from the lateral geniculate nucleus (LGN) and lateral posterior nucleus (LPN), the response selectivity of the V1 neurons could be influenced mostly by these inputs. However, it remains unclear how these two thalamic inputs contribute to the response selectivity of the V1 neurons. In this study, we examined the orientation, direction and spatial frequency selectivity of the LPN axons projecting to V1 and compared their response selectivity with our previous results of the LGN axons in mice. For this purpose, the genetically encoded calcium indicator, GCaMP6s, was locally expressed in the LPN using the adeno-associated virus (AAV) infection method. Visual stimulations were presented, and axonal imaging was conducted in V1 by two-photon calcium imaging in vivo. We found that LPN axons primarily terminate in layers 1 and 5 and, to a lesser extent, in layers 2/3 and 4 of V1, while LGN axons mainly terminate in layer 4 and, to a lesser extent, in layers 1 and 2/3 of V1. LPN axons send highly orientation- and direction-selective inputs to all the examined layers in V1, whereas LGN axons send highly orientation- and direction-selective inputs to layers 1 and 2/3 but low orientation and direction selective inputs to layer 4 in V1. The distribution of preferred orientation and direction was strongly biased toward specific orientations and directions in LPN axons, while weakly biased to cardinal orientations and directions in LGN axons. In spatial frequency tuning, both the LPN and LGN axons send selective inputs to V1. The distribution of preferred spatial frequency was more diverse in the LPN axons than in the LGN axons. In conclusion, LPN inputs to V1 are functionally different from LGN inputs and may have different roles in the orientation, direction and spatial frequency tuning of the V1 neurons.

Dataset Information

Hierarchical stimulus processing in rodent primary and lateral visual cortex as assessed through neuronal selectivity and repetition suppression.

Publications

Hierarchical stimulus processing in rodent primary and lateral visual cortex as assessed through neuronal selectivity and repetition suppression.

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