Deep Cortical Layers Are Activated Directly by Thalamus

Constantinople, Christine M.; Bruno, Randy M.

doi:10.1126/science.1236425

Cited by 422 publications

(436 citation statements)

References 35 publications

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“…Sensory information from the thalamus largely targets the intermediate layer 4 and sparsely targets the layer 5/6 border (23,24). From layer 4, axonal projections go to the superficial layers 2/3 and then to the deep layers 5/6, where information is distributed to other cortical and subcortical targets (23,25).…”

Section: Resultsmentioning

confidence: 99%

Coding principles of the canonical cortical microcircuit in the avian brain

Calabrese

Woolley

2015

Proc. Natl. Acad. Sci. U.S.A.

113

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Mammalian neocortex is characterized by a layered architecture and a common or "canonical" microcircuit governing information flow among layers. This microcircuit is thought to underlie the computations required for complex behavior. Despite the absence of a six-layered cortex, birds are capable of complex cognition and behavior. In addition, the avian auditory pallium is composed of adjacent information-processing regions with genetically identified neuron types and projections among regions comparable with those found in the neocortex. Here, we show that the avian auditory pallium exhibits the same information-processing principles that define the canonical cortical microcircuit, long thought to have evolved only in mammals. These results suggest that the canonical cortical microcircuit evolved in a common ancestor of mammals and birds and provide a physiological explanation for the evolution of neural processes that give rise to complex behavior in the absence of cortical lamination.functional connectivity | cortex evolution | songbird | sensory coding T he cognitive abilities of birds suggest that the avian brain contains sophisticated information-processing circuitry. Recent studies have demonstrated that corvids, such as crows, rooks, and jays, exhibit innovative tool manufacture (1), referential gesturing (2), causal reasoning (3, 4), mirror self-recognition (5), and planning for future needs using recent experience (6). Other birds can perform complex pattern recognition (7), long-term recollection (8), and numerical discrimination (9), paralleling the performance of primates. Songbirds, such as zebra finches (Taeniopygia guttata, the species studied here), learn to produce and recognize complex vocalizations for social communication, with numerous parallels to speech learning and perception (10).Although cognitive skills in birds and nonhuman mammals are often comparable, avian and mammalian palliums exhibit very different anatomical organization. Although the organization of ascending sensory pathways and subpallial structures are similar in avian and mammalian brains (11), the avian pallium (referred to hereafter as the cortex) lacks the distinctive six-layered structure of the mammalian neocortex (12). Instead of a laminar structure, the avian cortex is composed of interconnected nuclei and bands of neurons that form distinct processing regions. The avian primary auditory cortex (avian A1) is organized into adjacent processing regions, collectively called the field L/CM (caudal mesopallium) complex, that are stacked in a dorsorostral to ventrocaudal orientation (13, 14) ( Fig. 1 and Fig. S1). Regions of avian A1 are delineated by differences in cytoarchitecture and connectivity (13, 15) (SI Materials and Methods) and are organized into superficial (field L1 and lateral caudal mesopallium, CML), intermediate (field L2a and -b), and deep (field L3) regions, similar to neocortical layers. A posterior region, the caudal nidopallium (NC) is referred to as "secondary" cortex here. Fig. 2A shows a schemati...

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Section: Resultsmentioning

confidence: 99%

Coding principles of the canonical cortical microcircuit in the avian brain

Calabrese

Woolley

2015

Proc. Natl. Acad. Sci. U.S.A.

113

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“…Sensory information about appetitive CSs may reach the Te2 cortex via layers II/III, which is connected to the Te1 auditory cortex (Romanski and LeDoux 1993a) and which also receives some sparse afferents from subcortical nuclei. In addition, a recent study showed that thalamic inputs to the cortex terminate also in the layer V/VI (Constantinople and Bruno 2013), two of the layers in which we found enhanced activity after memory retrieval.…”

Section: Layer IVmentioning

confidence: 94%

Region- and Layer-Specific Activation of the Higher Order Auditory Cortex Te2 after Remote Retrieval of Fear or Appetitive Memories

et al. 2016

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The auditory cortex is involved in encoding sounds which have acquired an emotional-motivational charge. However, the neural circuitry engaged by emotional memory processes in the auditory cortex is poorly understood. In this study, we investigated the layers and regions that are recruited in the higher order auditory cortex Te2 by a tone previously paired to either fear or appetitive stimuli in rats. By tracking the protein coded by the immediate early gene zif268, we found that fear memory retrieval engages layers II-III in most regions of Te2. These results were neither due to an enhanced fear state nor to fear-evoked motor responses, as they were absent in animals retrieving an olfactory fear memory. These layers were also activated by appetitive auditory memory retrieval. Strikingly, layer IV was recruited by fear, but not appetitive memories, whereas layer V activity was related to the behavioral responses displayed to the CS.In addition to revealing the layers and regions which are recruited in the Te2 by either fear or appetitive remote memories, our study also shows that the neural circuitry within the Te2 that processes and stores emotional memories varies on the basis of the affective-motivational charge of tones.

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“…resting-state fMRI | thalamus | preterm | functional connectivity | cortex T he formation of topographically organized neural connections between cerebral cortex and thalamus is necessary for normal cortical morphogenesis (1), and development of these connections requires thalamocortical projections to synapse transiently in the temporary cortical subplate before penetrating the cortical plate (2)(3)(4). In humans, the subplate is at maximal extent in the last trimester of gestation (5), a time of rapid growth for thalamocortical fibers and the cortical dendritic tree, particularly in heteromodal cortex (6,7).…”

mentioning

confidence: 99%

Specialization and integration of functional thalamocortical connectivity in the human infant

Toulmin

Beckmann

O’Muircheartaigh

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

149

148

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Connections between the thalamus and cortex develop rapidly before birth, and aberrant cerebral maturation during this period may underlie a number of neurodevelopmental disorders. To define functional thalamocortical connectivity at the normal time of birth, we used functional MRI (fMRI) to measure blood oxygen level-dependent (BOLD) signals in 66 infants, 47 of whom were at high risk of neurocognitive impairment because of birth before 33 wk of gestation and 19 of whom were term infants. We segmented the thalamus based on correlation with functionally defined cortical components using independent component analysis (ICA) and seed-based correlations. After parcellating the cortex using ICA and segmenting the thalamus based on dominant connections with cortical parcellations, we observed a near-facsimile of the adult functional parcellation. Additional analysis revealed that BOLD signal in heteromodal association cortex typically had more widespread and overlapping thalamic representations than primary sensory cortex. Notably, more extreme prematurity was associated with increased functional connectivity between thalamus and lateral primary sensory cortex but reduced connectivity between thalamus and cortex in the prefrontal, insular and anterior cingulate regions. This work suggests that, in early infancy, functional integration through thalamocortical connections depends on significant functional overlap in the topographic organization of the thalamus and that the experience of premature extrauterine life modulates network development, altering the maturation of networks thought to support salience, executive, integrative, and cognitive functions.resting-state fMRI | thalamus | preterm | functional connectivity | cortex T he formation of topographically organized neural connections between cerebral cortex and thalamus is necessary for normal cortical morphogenesis (1), and development of these connections requires thalamocortical projections to synapse transiently in the temporary cortical subplate before penetrating the cortical plate (2-4). In humans, the subplate is at maximal extent in the last trimester of gestation (5), a time of rapid growth for thalamocortical fibers and the cortical dendritic tree, particularly in heteromodal cortex (6, 7). This process has been shown to be disrupted by preterm birth (8). Premature delivery is associated with increased risk of neurocognitive impairment, and it is widely hypothesized that abnormal development of brain structure during this period is the cause of these problems and may also underlie the development of autistic spectrum disorders and attention deficit disorders in genetically predisposed individuals.During the last trimester of pregnancy, functional MRI (fMRI) detects the emergence of coordinated, spontaneous fluctuations in the blood oxygen level-dependent (BOLD) signals, which are closely linked with the development of electroencephalographic activity (9-11) and develop into a near-facsimile of the mature adult resting-state network architecture by the...

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Deep Cortical Layers Are Activated Directly by Thalamus

Cited by 422 publications

References 35 publications

Coding principles of the canonical cortical microcircuit in the avian brain

Coding principles of the canonical cortical microcircuit in the avian brain

Region- and Layer-Specific Activation of the Higher Order Auditory Cortex Te2 after Remote Retrieval of Fear or Appetitive Memories

Specialization and integration of functional thalamocortical connectivity in the human infant

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