scholarly journals Three rules govern thalamocortical connectivity of fast-spike inhibitory interneurons in the visual cortex

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Yulia Bereshpolova ◽  
Xiaojuan Hei ◽  
Jose-Manuel Alonso ◽  
Harvey A Swadlow

Some cortical neurons receive highly selective thalamocortical (TC) input, but others do not. Here, we examine connectivity of single thalamic neurons (lateral geniculate nucleus, LGN) onto putative fast-spike inhibitory interneurons in layer 4 of rabbit visual cortex. We show that three ‘rules’ regulate this connectivity. These rules concern: (1) the precision of retinotopic alignment, (2) the amplitude of the postsynaptic local field potential elicited near the interneuron by spikes of the LGN neuron, and (3) the interneuron’s response latency to strong, synchronous LGN input. We found that virtually all first-order fast-spike interneurons receive input from nearly all LGN axons that synapse nearby, regardless of their visual response properties. This was not the case for neighboring regular-spiking neurons. We conclude that profuse and highly promiscuous TC inputs to layer-4 fast-spike inhibitory interneurons generate response properties that are well-suited to mediate a fast, sensitive, and broadly tuned feed-forward inhibition of visual cortical excitatory neurons.

2018 ◽  
Vol 120 (5) ◽  
pp. 2218-2231
Author(s):  
Eduard Maier ◽  
Michael Brecht

Bodies change continuously, but we do not know if and how these changes affect somatosensory cortex. We address this issue in the whisker-barrel-cortex-pathway. We ask how outgrowing whiskers are mapped onto layer 4 barrel neuron responses. Half of whisker follicles contained dual whiskers, a shorter presumably outgrowing whisker (referred to as young whisker) and a longer one (referred to as old whisker). Young whiskers were much thinner than old ones but were inserted more deeply into the whisker follicle. Both whiskers were embedded in one outer root sheath surrounded by a common set of afferent nerve fibers. We juxtacellularly identified layer 4 barrel neurons representing dual whiskers with variable whisker length differences in anesthetized rats. Strength and latency of neuronal responses were strongly correlated for deflections of young and old whiskers but were not correlated with whisker length. The direction preferences of young and old whiskers were more similar than expected by chance. Old whiskers evoked marginally stronger and slightly shorter latency spike and local field potential responses than young whiskers. Our data suggest a conservative rewiring mechanism, which connects young whiskers to existing peripheral sensors. The fact that layer 4 barrel neurons retain their response properties is remarkable given the different length, thickness, and insertion depth of young and old whiskers. Retention of cortical response properties might be related to the placement of young and old whisker in one common outer root sheath and may contribute to perceptual stability across whisker replacement. NEW & NOTEWORTHY A particularly dramatic bodily change is whisker regrowth, which involves the formation of dual whisker follicles. Our results suggest that both whiskers are part of the same mechanoreceptive unit. Despite their distinct whisker length and thickness, responses of single cortical neurons to young and old whisker deflection were similar in strength, latency, and directional tuning. We suggest the congruence of young and old whisker cortical responses contributes to perceptual stability over whisker regrowth.


1978 ◽  
Vol 41 (6) ◽  
pp. 1466-1494 ◽  
Author(s):  
R. W. Rhoades ◽  
L. M. Chalupa

1. In normal hamsters the visual cortex sends a retinotopically organized projection to the ipsilateral superior colliculus. 2. Acute or chronic unilateral ablations of visual cortex in adult animals decrease the incidence of directionally selective cells encountered in the superficial laminae of the ipsilateral colliculus, but not in the deeper layers (those ventral to the stratum opticum). 3. Unilateral ablations of visual cortex in infant hamsters induce an aberrant crossed projection to the contralateral superior colliculus, confirming the finding of Mustari and Lund (58) in the rat. Horseradish peroxidase (HRP) experiments demonstrated that the cells whose axons comprise the normal as well as the anomalous projection are pyramidal neurons in layer V of cortex. 4. In adult hamsters that underwent early brain damage, about 13% of the cells in the colliculus could be activated by stimulation of the contralateral visual cortex. Only 1 unit (of the 159 cells tested) could be driven by similar stimulation in normal adult hamsters. This indicates that the anomalous crossed projection forms functional synapses in the contralateral tectum. 5. No cells (of the 113 tested) could be activated from the contralateral cortex in hamsters that sustained chronic ablations of visual cortex in adulthood; thus indicating that there is some limited time period during development when unilateral ablations of visual cortex induce an anomalous corticotectal pathway. 6. The visual response properties of superior collicular neurons in the neonatally brain-damaged animals were compared to those of normal hamsters, as well as to those with acute or chronic ablations of visual cortex sustained in adulthood. 7. There was no indication that the anomalous projection contributes to the organization of normal visual response properties in the superior colliculus of the neonatally brain-damaged animals. In fact, the incidence of directionally selective cells in these hamsters was found to be significantly lower than that of normals in both the superficial and deep laminae of the colliculus. 8. We conclude that while unilateral damage of visual cortex in the hamster induces an anomalous corticotectal projection that makes functional synapses, this aberrant input does not compensate for missing, normal corticotectal pathway in the organization of superior collicular response properties.


2013 ◽  
Vol 33 (28) ◽  
pp. 11372-11389 ◽  
Author(s):  
J. Zhuang ◽  
C. R. Stoelzel ◽  
Y. Bereshpolova ◽  
J. M. Huff ◽  
X. Hei ◽  
...  

2020 ◽  
Author(s):  
Lukas Klimmasch ◽  
Johann Schneider ◽  
Alexander Lelais ◽  
Bertram E. Shi ◽  
Jochen Triesch

AbstractThe development of binocular vision is an active learning process comprising the development of disparity tuned neurons in visual cortex and the establishment of precise vergence control of the eyes. We present a computational model for the learning and self-calibration of active binocular vision based on the Active Efficient Coding framework, an extension of classic efficient coding ideas to active perception. Under normal rearing conditions, the model develops disparity tuned neurons and precise vergence control, allowing it to correctly interpret random dot stereogramms. Under altered rearing conditions modeled after neurophysiological experiments, the model qualitatively reproduces key experimental findings on changes in binocularity and disparity tuning. Furthermore, the model makes testable predictions regarding how altered rearing conditions impede the learning of precise vergence control. Finally, the model predicts a surprising new effect that impaired vergence control affects the statistics of orientation tuning in visual cortical neurons.


2017 ◽  
Vol 117 (2) ◽  
pp. 566-581 ◽  
Author(s):  
James C. Dooley ◽  
Michaela S. Donaldson ◽  
Leah A. Krubitzer

The functional organization of the primary visual area (V1) and the importance of sensory experience in its normal development have been well documented in eutherian mammals. However, very few studies have investigated the response properties of V1 neurons in another large class of mammals, or whether sensory experience plays a role in shaping their response properties. Thus we reared opossums ( Monodelphis domestica) in normal and vertically striped cages until they reached adulthood. They were then anesthetized using urethane, and electrophysiological techniques were used to examine neuronal responses to different orientations, spatial and temporal frequencies, and contrast levels. For normal opossums, we observed responses to the temporal and spatial characteristics of the stimulus to be similar to those described in small, nocturnal, eutherian mammals such as rats and mice; neurons in V1 responded maximally to stimuli at 0.09 cycles per degree and 2.12 cycles per second. Unlike other eutherians, but similar to other marsupials investigated, only 40% of the neurons were orientation selective. In stripe-reared animals, neurons were significantly more likely to respond to vertical stimuli at a wider range of spatial frequencies, and were more sensitive to gratings at lower contrast values compared with normal animals. These results are the first to demonstrate experience-dependent plasticity in the visual system of a marsupial species. Thus the ability of cortical neurons to alter their properties based on the dynamics of the visual environment predates the emergence of eutherian mammals and was likely present in our earliest mammalian ancestors.NEW & NOTEWORTHY These results are the first description of visual response properties of the most commonly studied marsupial model organism, the short-tailed opossum ( Monodelphis domestica). Further, these results are the first to demonstrate experience-dependent plasticity in the visual system of a marsupial species. Thus the ability of cortical neurons to alter their properties based on the dynamics of the visual environment predates the emergence of eutherian mammals and was likely present in our earliest mammalian ancestors.


2008 ◽  
Vol 100 (3) ◽  
pp. 1476-1487 ◽  
Author(s):  
Bin Zhang ◽  
Earl L. Smith ◽  
Yuzo M. Chino

Vision of newborn infants is limited by immaturities in their visual brain. In adult primates, the transient onset discharges of visual cortical neurons are thought to be intimately involved with capturing the rapid succession of brief images in visual scenes. Here we sought to determine the responsiveness and quality of transient responses in individual neurons of the primary visual cortex (V1) and visual area 2 (V2) of infant monkeys. We show that the transient component of neuronal firing to 640-ms stationary gratings was as robust and as reliable as in adults only 2 wk after birth, whereas the sustained component was more sluggish in infants than in adults. Thus the cortical circuitry supporting onset transient responses is functionally mature near birth, and our findings predict that neonates, known for their “impoverished vision,” are capable of initiating relatively mature fixating eye movements and of performing in detection of simple objects far better than traditionally thought.


1991 ◽  
Vol 66 (1) ◽  
pp. 293-306 ◽  
Author(s):  
L. J. Larson-Prior ◽  
P. S. Ulinski ◽  
N. T. Slater

1. A preparation of turtle (Chrysemys picta and Pseudemys scripta) brain in which the integrity of the intracortical and geniculocortical pathways in visual cortex are maintained in vitro has been used to differentiate the excitatory amino acid (EAA) receptor subtypes involved in geniculocortical and intracortical synapses. 2. Stimulation of the geniculocortical fibers at subcortical loci produces monosynaptic excitatory postsynaptic potentials (EPSPs) in visual cortical neurons. These EPSPs are blocked by the broad-spectrum EAA receptor antagonist kynurenate (1-2 mM) and the non-N-methyl-D-aspartate (NMDA) antagonist 6, 7-dinitroquinoxaline-2,3-dione (DNQX, 10 microM), but not by the NMDA antagonist D,L-2-amino-5-phosphonovalerate (D,L-AP-5, 100 microM). These results indicate that the geniculocortical EPSP is mediated by EAAs that access principally, if not exclusively, EAA receptors of the non-NMDA subtypes. 3. Stimulation of intracortical fibers evokes compound EPSPs that could be resolved into three components differing in latency to peak. The component with the shortest latency was not affected by any of the EAA-receptor antagonists tested. The second component, of intermediate latency, was blocked by kyurenate and DNQX but not by D,L-AP-5. The component of longest latency was blocked by kynurenate and D,L-AP-5, but not by DNQX. These results indicate that the compound intracortical EPSP is comprised of three pharmacologically distinct components that are mediated by an unknown receptor, by quisqualate/kainate, and by NMDA receptors, respectively. 4. Repetitive stimulation of intracortical pathways at 0.33 Hz produces a dramatic potentiation of the late, D,L-AP-5-sensitive component of the intracortical EPSP. 5. These experiments lead to a hypothesis about the subtypes of EAA receptors that are accessed by the geniculocortical and intracortical pathways within visual cortex.


2019 ◽  
Author(s):  
Kyle R. Jenks ◽  
Jason D. Shepherd

ABSTRACTThe normal development of neuronal circuits requires both hard-wired gene expression and experience. Sensory processing, such as vision, is especially sensitive to perturbations in experience. However, the exact contribution of experience to neuronal visual response properties and binocular vision remains unknown. To determine how visual response properties developin vivo, we used single cell resolution two-photon calcium imaging of mouse binocular visual cortex at multiple time-points after eye opening. Few neurons are binocularly responsive immediately after eye opening and respond solely to either the contralateral or ipsilateral eye. Binocular neurons emerge during development, which requires visual experience, and show specific tuning of visual response properties. As binocular neurons emerge, activity between the two eyes becomes more correlated in the neuropil. Since experience-dependent plasticity requires the expression of activity-dependent genes, we determined whether the plasticity geneArcmediates the development of normal visual response properties. Surprisingly, rather than mirroring the effects of visual deprivation, mice that lackArcshow increased numbers of binocular neurons during development. Strikingly, removingArcin adult binocular visual cortex increases the numbers of binocular neurons and recapitulates the developmental phenotype, suggesting cortical circuits that mediate visual processing require ongoing experience-dependent plasticity. Thus, experience is critical for the normal development and maintenance of circuits required to process binocular vision.


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