Characteristics of corticothalamic neurons in area 17 of the cat

Harvey, A.R.

doi:10.1016/0304-3940(78)90164-7

Cited by 43 publications

(29 citation statements)

References 16 publications

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“…Anatomical and physiological evidence from a variety of mammalian species support different organizational schemes for CG circuits, including evidence that CG circuits are comprised of multiple distinct cell types suggestive of stream-specific organization (Briggs and Callaway, 2001; Briggs and Usrey, 2007, 2009; Conley and Raczkowski, 1990; Fitzpatrick et al, 1994; Harvey, 1978; Ichida and Casagrande, 2002; Lund et al, 1975; Swadlow and Weyand, 1987; Tsumoto and Suda, 1980; Usrey and Fitzpatrick, 1996; Wiser and Callaway, 1996) and evidence that CG circuits are comprised of homogeneous cell types suggestive of feedback to overlapping LGN layers (Ichida et al, 2014; Katz, 1987). Due to sparse CG neuron distributions (in the macaque monkey, only ~14% of layer 6 neurons are CG neurons (Fitzpatrick et al, 1994)) and potential biases of traditional anatomical and physiological measurements toward more common CG cell types, the precise structural organization of CG feedback has been difficult to establish.…”

Section: Discussionmentioning

confidence: 99%

“…Physiological recordings of CG neurons in alert primates reveal distinct CG cell types carrying information related to the magnocellular, parvocellular, or koniocellular feedforward processing streams (Briggs and Usrey, 2009, 2011). Likewise, physiological studies examining CG neurons in carnivores and rabbits also conclude that the CG feedback pathway is comprised of functionally distinct neurons (Briggs and Usrey, 2005; Grieve and Sillito, 1995; Harvey, 1978; Swadlow and Weyand, 1987; Tsumoto and Suda, 1980). Thus while anatomical evidence suggests that CG circuits may not be strictly stream-specific (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey

Briggs

Kiley

Callaway

et al. 2016

Neuron

111

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Corticothalamic circuits are essential for reciprocal information exchange between the thalamus and cerebral cortex. Nevertheless, the role of corticothalamic circuits in sensory processing remains a mystery. In the visual system, afferents from retina to the lateral geniculate nucleus (LGN) and from LGN to primary visual cortex (V1) are organized into functionally distinct parallel processing streams. Physiological evidence suggests corticogeniculate feedback may be organized into parallel streams; however, little is known about the diversity of corticogeniculate neurons, their local computations, or the structure-function relationship among corticogeniculate neurons. We used a virus-mediated approach to label and reconstruct the complete dendritic and local axonal arbors of identified corticogeniculate neurons in the macaque monkey. Our results reveal morphological substrates for parallel streams of corticogeniculate feedback based on distinct classes of neurons in V1 and V2. These results support the hypothesis that distinct populations of feedback neurons provide independent and unique information to the LGN.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey

Briggs

Kiley

Callaway

et al. 2016

Neuron

111

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“…Thus, particular features of a visual scene could trigger CG activation, causing streamspecific feedback activation of LGN ensembles via the circuit mechanism described above. Interestingly, CG feedback in a variety of species is known to operate on different timescales due to differential axon conduction velocities among the diverse CG neuronal types (35,44,(47)(48)(49)(50)(51). The large variation in axon conduction times suggests that different CG neurons may have shorter or longer timescales over which they can integrate incoming information.…”

Section: Discussionmentioning

confidence: 99%

Corticogeniculate feedback sharpens the temporal precision and spatial resolution of visual signals in the ferret

Hasse

Briggs

2017

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

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The corticogeniculate (CG) pathway connects the visual cortex with the visual thalamus (LGN) in the feedback direction and enables the cortex to directly influence its own input. Despite numerous investigations, the role of this feedback circuit in visual perception remained elusive. To probe the function of CG feedback in a causal manner, we selectively and reversibly manipulated the activity of CG neurons in anesthetized ferrets in vivo using a combined viral-infection and optogenetics approach to drive expression of channelrhodopsin2 (ChR2) in CG neurons. We observed significant increases in temporal precision and spatial resolution of LGN neuronal responses to drifting grating and white noise stimuli when CG neurons expressing ChR2 were light activated. Enhancing CG feedback reduced visually evoked response latencies, increased spike-timing precision, and reduced classical receptive field size. Increased precision among LGN neurons led to increased spike-timing precision among granular layer V1 neurons as well. Together, our findings suggest that the function of CG feedback is to control the timing and precision of thalamic responses to incoming visual signals.T he feedforward progression of sensory information from peripheral receptors through nuclei in the sensory thalamus to the primary sensory cortex is well understood. For example, much is known about how neurons in the primary sensory cortex represent elementary sensory features based on the inputs they receive from peripheral and thalamic neurons with well-defined receptive field properties. In addition to these feedforward circuits, mammalian sensory systems include a substantial feedback projection from the primary sensory cortex to the sensory thalamus (1). Despite a rich history of investigation, the functional role of corticothalamic feedback circuits in sensory perception remains a fundamental mystery in neuroscience.Our goal was to determine the functional contribution of corticothalamic feedback to vision. Corticogeniculate (CG) circuits link the primary visual cortex (V1) with the lateral geniculate nucleus of the thalamus (LGN) and constitute the first cortical feedback connection in the visual processing hierarchy (2). CG axons target LGN relay neurons, local interneurons within the LGN, and neurons in the visual portion of the thalamic reticular nucleus (TRN) that inhibit LGN relay neurons (3-5) (Fig. 1A). Based on this pattern of axonal innervation, CG modulation of LGN neurons could include both monosynaptic excitation and disynaptic inhibition of LGN relay neurons via TRN and/or local LGN inhibitory circuitry. The CG circuit is anatomically robust-cortical synapses onto LGN relay neurons far outnumber retinal synapses (4); however, the receptive fields of LGN relay neurons reflect their retinal and not their cortical inputs (6). In part due to its subtle influence on LGN responses, the function of CG feedback has remained elusive.There have been numerous experimental examinations of CG function-using methods with varying degrees of sele...

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“…In the light of this finding, the fact that most corticothalamic neurons have simple RFs (Harvey, 1978(Harvey, , 1980Ferster and Lindström, 1983;Martin and Whitteridge, 1984;Grieve and Sillito, 1995) (but see Gilbert, 1977) raises additional questions, because it is generally assumed that simple cells are created by their thalamic input (Hubel and Wiesel, 1962;Bullier et al, 1982;Tanaka, 1983;Ferster, 1987;Reid and Alonso, 1995;Alonso et al, 2001;Hirsch and Martinez, 2006). dLGN and simple receptive fields of corticothalamic neurons How many thalamic synapses are necessary to generate the simple RF?…”

Section: Discussionmentioning

confidence: 99%

“…In this study we investigated the pattern of thalamic input to the layer 6 corticothalamic (CT) pyramidal cells, which are unusual in having dendrites in two thalamorecipient layers: basal dendrites in layer 6 and apical dendrites in layer 4. The CT cells can be monosynaptically excited by electrical stimulation of the thalamic relay cells (Gilbert, 1977;Ferster and Lindström, 1983;Martin and Whitteridge, 1984) and, like neurons in layer 4, most have simple receptive fields (Harvey, 1978(Harvey, , 1980Ferster and Lindström, 1983;Martin and Whitteridge, 1984;Grieve and Sillito, 1995) (but see Gilbert, 1977). In addition to their feedback to the thalamus, CT cells send a collateral projection to layer 4, where they form an estimated 9 -19 times more synapses than the thalamic afferents (Ahmed et al, 1994;Binzegger et al, 2004), mainly with spiny neurons (McGuire et al, 1984;Ahmed et al, 1994;Anderson et al, 1994;Binzegger et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Selective Targeting of the Dendrites of Corticothalamic Cells by Thalamic Afferents in Area 17 of the Cat

Costa¹,

Martin²

2009

J. Neurosci.

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Pyramidal cells of layer 6 in cat visual cortex are the source of the corticothalamic projection, and their recurrent collaterals provide substantially more excitatory synapses in layer 4 than does the thalamic input. They have predominantly simple receptive fields and can be driven monosynaptically by electrically stimulating thalamic relay cells. Layer 6 cells could thus provide a significant disynaptic amplification of the thalamic input to layer 4, particularly since their synapses facilitate, unlike the thalamic afferents whose synapses depress. However, purely geometric considerations of the relation of their dendritic trees to the thalamic input indicate that they should form a far smaller number of synapses with thalamic afferents than do the simple cells of layer 4. We thus analyzed quantitatively the thalamic input to identified corticothalamic cells by labeling the thalamic afferents and corticothalamic cells in vivo. We made a correlated light and electron microscopic study of 73 "contacts" between thalamic afferents and five corticothalamic cells. The electron microscope revealed that only 24 of the contacts identified at light microscope level were indeed synapses and, contrary to geometric predictions, virtually all were located on spines on the basal dendrites. Our quantitative estimates indicate that the corticothalamic cells form even fewer synapses with the thalamic afferents than predicted by geometric considerations and only 1/10 as many as do the layer 4 simple cells. These data strongly suggest it is the collective computation of cortical neurons, not the monosynaptic thalamic input, that determines the output of the corticothalamic cells.

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Characteristics of corticothalamic neurons in area 17 of the cat

Cited by 43 publications

References 16 publications

Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey

Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey

Corticogeniculate feedback sharpens the temporal precision and spatial resolution of visual signals in the ferret

Selective Targeting of the Dendrites of Corticothalamic Cells by Thalamic Afferents in Area 17 of the Cat

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