Unique Functional Properties of On and Off Pathways in the Developing Mammalian Retina

Wang, Guoyong; Liets, Lauren C.; Chalupa, Leo M.

doi:10.1523/jneurosci.21-12-04310.2001

Cited by 62 publications

(65 citation statements)

References 41 publications

(67 reference statements)

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“…9). These data did not indicate dramatic rearrangements in On and Off pathways over this period but, like previous recordings from the retina (Wang et al, 2001), suggest that On and Off may not be fully mature at the onset of visual responsiveness. It remains to be shown exactly which features of spontaneous and visually evoked activity contribute to the emergence and maintenance of On and Off pathways as development progresses.…”

Section: Relevance To the Maturation Of Circuitssupporting

confidence: 78%

“…Physiological and anatomical data show that at this stage the dendrites of a significant fraction of ferret RGCs are not completely stratified into either the On or Off sublamina of the inner plexiform layer (Wang et al, 2001). However, even before eye opening in the ferret, On-dominated and Off-dominated cell activity is strongly patterned under natural viewing conditions, with cells of the same type showing correlated activity but cells of different type showing anticorrelated activity (Akerman et al, 2002).…”

Section: Relevance To the Maturation Of Circuitsmentioning

confidence: 93%

“…Other data have suggested that the On and Off pathways in the retinogeniculate pathway are not fully mature by the onset of visual responsiveness but develop over a longer period of time, which includes the period before eye opening (Bodnarenko et al, 1999;Wang et al, 2001;Tian and Copenhagen, 2003). Physiological and anatomical data show that at this stage the dendrites of a significant fraction of ferret RGCs are not completely stratified into either the On or Off sublamina of the inner plexiform layer (Wang et al, 2001).…”

Section: Relevance To the Maturation Of Circuitsmentioning

confidence: 97%

“…In the period immediately after the onset of visual responsiveness, neuronal connections continue to change and refine in the ferret primary visual pathway. The maturation of On and Off pathways continues (Bodnarenko et al, 1999;Wang et al, 2001), and there are changes in the RF properties of visual neurons (Krug et al, 2001;White et al, 2001). What information could early visual responses provide that is relevant to these developing connections?…”

Section: Relevance To the Maturation Of Circuitsmentioning

confidence: 99%

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Spatial and Temporal Properties of Visual Responses in the Thalamus of the Developing Ferret

Akerman¹,

Grubb²,

Thompson³

2004

J. Neurosci.

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Spatiotemporal patterning of neural activity is thought to influence the development of connections in the visual pathway. This patterning can arise spontaneously or through sensory experience. Here, we use a combination of natural and simple stimuli to investigate which elements of the visual environment modulate the earliest responses in the primary visual pathway of developing ferrets. Recordings were made during the first 2 weeks of visual responsiveness, which, in the ferret, overlaps with the period that the eyelids have not yet opened. Even when the eyelids are closed, both thalamic and cortical activity was found to be temporally modulated under conditions of natural visual stimulation. The modulations correlated with temporal changes in stimulus contrast but also reflected spatial structure in the visual scene. Simple stimuli were used to show that early responses to naturalistic stimuli are influenced by the localization and structure of through-the-eyelid receptive fields. The early visual responses were also characterized by substantial variability in the ability of the cells to detect stimuli of different duration and different intensity, in a temporally precise manner. These temporal and spatial properties should constrain how plasticity mechanisms interpret naturally patterned activity. Key words: visual development; natural scenes; dLGN; response properties; ferret; closed eyelids IntroductionIt is well established that early visual experience is important for the development of the primary visual pathway (Katz and Shatz, 1996). Furthermore, manipulation experiments in vivo indicate that the spatiotemporal properties of neural activity can instruct the refinement of connections in the visual system (Hubel and Wiesel, 1965;Sengpiel et al., 1999;Engert et al., 2002;Ruthazer et al., 2003). For instance, artificially induced strabismus, which effectively decorrelates the inputs from the two eyes, disrupts the cortical connections that subserve binocularity (Hubel and Wiesel, 1965), and artificially correlating all neural activity in the optic nerves of ferrets in the period immediately before, and after, eye opening leads to abnormal development of orientation selectivity in visual cortex (Weliky and Katz, 1997). Other features of the visual system seem to develop normally when sources of activity are removed (Crowley and Katz, 1999) or when spatiotemporal patterns within the neural activity are disrupted (Huberman et al., 2003). However, the evidence that patterned neural activity can be used in an instructive way to refine connections has become central to models of neural development (Stent, 1971;Miller, 1994;Shouval et al., 1997).Inherent in these developmental models is the notion that the "fidelity" of the spatiotemporal patterned activity dictates which neurons are coactive and that this constrains the level of specificity that can be attained. However, although the quantitative properties of spontaneous activity in the developing retina (Meister et al., 1991;Wong and Oakley, 1996;Feller et al...

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Section: Relevance To the Maturation Of Circuitssupporting

confidence: 78%

Section: Relevance To the Maturation Of Circuitsmentioning

confidence: 93%

Section: Relevance To the Maturation Of Circuitsmentioning

confidence: 97%

Section: Relevance To the Maturation Of Circuitsmentioning

confidence: 99%

See 2 more Smart Citations

Spatial and Temporal Properties of Visual Responses in the Thalamus of the Developing Ferret

Akerman¹,

Grubb²,

Thompson³

2004

J. Neurosci.

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“…T ypically, sublamina b comprises the inner three-fifths of the I PL and sublamina a comprises the outer two-fifths of the I PL (Nelson et al, 1978). Stratified ␤ RGC s are present in the ferret retina for both age groups included in our study (Wong and Oakley, 1996;Wang et al, 2001). Figure 1a is an example of a pair of P21 ferret ␤ cells that were dye-filled with sulf urhodamine 101 (1%; Molecular Probes, Eugene, OR); their dendritic arbors were clearly separated, ramif ying in either sublamina a (OFF) or b (ON).…”

Section: Morphological Identification Of On and Off Rgcsmentioning

confidence: 91%

Mechanisms Underlying Developmental Changes in the Firing Patterns of ON and OFF Retinal Ganglion Cells during Refinement of their Central Projections

Myhr¹,

Lukasiewicz

Wong³

2001

J. Neurosci.

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Patterned neuronal activity is implicated in the refinement of connectivity during development. Calcium-imaging studies of the immature ferret visual system demonstrated previously that functionally separate ON and OFF retinal ganglion cells (RGCs) develop distinct temporal patterns of spontaneous activity as their axonal projections undergo refinement. OFF RGCs become spontaneously more active compared with ON cells, resulting in a decrease in synchronous activity between these cell types. This change in ON and OFF activity patterns is suitable for driving the activity-dependent refinement of their axonal projections. Here, we used whole-cell and perforatedpatch recording techniques to elucidate the mechanisms that underlie the developmental alteration in the ON and OFF RGC activity patterns. First, we show that before the refinement period, ON and OFF RGCs have similar spike patterns; however, during the period of segregation, OFF RGCs demonstrate significantly higher spike rates relative to ON cells. With increasing age, OFF cells require less depolarization to reach their action potential threshold and fire more spikes in response to current injection compared with ON cells. In addition, spontaneous postsynaptic currents and potentials are greater in magnitude in OFF cells than ON cells. In contrast, before axonal refinement, there are no differences in the intrinsic excitability or synaptic drive onto ON and OFF cells. Together, our results show that developmental changes in ON and OFF RGC excitability and in the strength of their synaptic drives act together to reshape the spike patterns of these cells in a manner appropriate for the refinement of their connectivity.

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Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina

Stacy

Wong

2002

J of Comparative Neurology

102

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Ganglion cells of the mammalian retina undergo structural remodeling before their dendrites are confined to functionally distinct laminas within the inner plexiform layer. It has been proposed that cholinergic amacrine cells provide laminar cues that remodel ganglion cell dendrites, because their processes stratify before those of the ganglion cells. To address this possibility, it is necessary to know whether cholinergic cells contact all or only some classes of ganglion cells during development. We, therefore, used two-photon microscopy to simultaneously reconstruct the dendritic arbors of different classes of ganglion cells and terminal processes of cholinergic cells in neonatal mouse retina. We determined that, after birth, cholinergic cells contacted only a subset of ganglion cells. Large bistratified cells (LBCs), resembling direction selective ganglion cells in other species, had dendrites that fasciculated with the cholinergic plexuses. The LBCs received numerous presynaptic cholinergic contacts shortly after birth. In contrast, large monostratified cells (LMCs), ramifying outside the cholinergic plexuses at maturity, received few, if any, cholinergic contacts even at early stages when their dendrites overlapped with the cholinergic processes. These observations suggest that cholinergic cells provide laminar cues for only subsets of ganglion cells. They also indicate that the synaptic organization between amacrine and ganglion cells may be specified early in development.

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Unique Functional Properties of On and Off Pathways in the Developing Mammalian Retina

Cited by 62 publications

References 41 publications

Spatial and Temporal Properties of Visual Responses in the Thalamus of the Developing Ferret

Spatial and Temporal Properties of Visual Responses in the Thalamus of the Developing Ferret

Mechanisms Underlying Developmental Changes in the Firing Patterns of ON and OFF Retinal Ganglion Cells during Refinement of their Central Projections

Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina

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