Possible Roles of Spontaneous Waves and Dendritic Growth for Retinal Receptive Field Development

Bürgi, Pierre-Yves; Grzywacz, Norberto M.

doi:10.1162/neco.1997.9.3.533

Cited by 12 publications

(12 citation statements)

References 32 publications

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“…Figure 2 illustrates the working hypothesis we have developed to explain these developmental changes in RGC receptive fields. According to this hypothesis, the responses to multiple directions or orientations of motion in immature RGCs reflect polarised and poorly branched dendritic trees at these early stages, a possibility that has been addressed in theoretical studies (Burgi & Grzywacz, 1997). Alternatively these immature responses could be due to sparse synaptic connections onto immature dendrites rather than to the spatial layout of these same dendrites.…”

Section:     Rgc  mentioning

confidence: 99%

The role of early neural activity in the maturation of turtle retinal function

Sernagor

Mehta

2001

Journal of Anatomy

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In the developing vertebrate retina, ganglion cells fire spontaneous bursts of action potentials long before the eye becomes exposed to sensory experience at birth. These early bursts are synchronised between neighbouring retinal ganglion cells (RGCs), yielding unique spatiotemporal patterns : ' waves ' of activity sweep across large retinal areas every few minutes. Both at retinal and extraretinal levels, these embryonic retinal waves are believed to guide the wiring of the visual system using hebbian mechanisms of synaptic strengthening.In the first part of this review, we recapitulate the evidence for a role of these embryonic spontaneous bursts of activity in shaping developing complex receptive field properties of RGCs in the turtle embryonic retina. We also discuss the role of visual experience in establishing RGC visual functions, and how spontaneous activity and visual experience interact to bring developing receptive fields to maturation. We have hypothesised that the physiological changes associated with development reflect modifications in the dendritic arbours of RGCs, the anatomical substrate of their receptive fields. We demonstrate that there is a temporal correlation between the period of receptive field expansion and that of dendritic growth. Moreover, the immature spontaneous activity contributes to dendritic growth in developing RGCs. Intracellular staining of RGCs reveals, however, that immature receptive fields only rarely show direct correlation with the layout of the corresponding dendritic tree. To investigate the possibility that not only the presence of the spontaneous activity, but even the precise spatiotemporal patterns encoded in retinal waves might contribute to the refinement of retinal neural circuitry, first we must clarify the mechanisms mediating the generation and propagation of these waves across development. In the second part of this review, we present evidence that turtle retinal waves, visualised using calcium imaging, exhibit profound changes in their spatiotemporal patterns during development. From fast waves sweeping across large retinal areas and recruiting many cells on their trajectory at early stages, waves become slower and eventually stop propagating towards hatching, when they become stationary patches of neighbouring coactive RGCs. A developmental switch from excitatory to inhibitory GABA A responses appears to mediate the modification in spontaneous activity patterns while the retina develops. Future chronic studies using specific spatiotemporal alterations of the waves will shed a new light on how the wave dynamics help in sculpting retinal receptive fields.

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Section:     Rgc  mentioning

confidence: 99%

The role of early neural activity in the maturation of turtle retinal function

Sernagor

Mehta

2001

Journal of Anatomy

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“…In addition, spontaneous activity may have intraretinal significance. Previous studies have implicated activity in the development of dendritic morphology (Bodnarenko and Chalupa, 1993;Bodnarenko et al, 1995) and receptive field properties (Sernagor and Grzy wacz, 1996;Burgi and Grzy wacz, 1997). Thus, it is possible that spontaneous activity in RGC s may be relevant to establishing afferent, in addition to efferent, connections.…”

Section: What Can the Spatial And Temporal Patterns Of Spontaneous Acmentioning

confidence: 99%

Developmentally Regulated Spontaneous Activity in the Embryonic Chick Retina

1998

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Even before birth and the onset of sensory experience, neural activity plays an important role in shaping the vertebrate nervous system. In the embryonic chick visual system, activity in the retina before vision has been implicated in the refinement of retinotopic maps, the elimination of transient projections, and the survival of a full complement of neurons. In this study, we report the detection of a physiological substrate for these phenomena: waves of spontaneous activity in the ganglion cell layer of the embryonic chick retina. The activity is robust and highly patterned, taking the form of large amplitude, rhythmic, and wide-ranging waves of excitation that propagate across the retina. Activity waves are most prominent and organized between embryonic days 13-18, coinciding with the developmental period during which retinal axons refine their connections in their targets. The spatial and temporal features of the patterns observed are consistent with the role of activity patterns in shaping eye-specific projections and retinotopic maps but inconsistent with the hypothesis that they specify lamina-specific projections in the tectum. Antagonists of glutamatergic and glycinergic transmission and of gap junctional communication suppress spontaneous activity, whereas antagonists to GABAergic transmission potentiate it. Based on these results, we propose that spontaneous activity in the ganglion cells is regulated by chemical inputs from both bipolar and amacrine cells and by gap junctional coupling involving ganglion cells.

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“…Self-organizing neural networks can produce orientation-selective neurons after training with uncorrelated noise (Linsker, 1986;Burgi & Grzywacz, 1997). Smoothing uncorrelated and random noise by a Gaussian function produces a Gaussian correlation function.…”

Section: Models Based On the Exin And The Lissom Rulesmentioning

confidence: 99%

Models of receptive-field dynamics in visual cortex

Kalarickal

Marshall

1999

Vis Neurosci

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The position, size, and shape of the receptive field (RF) of some cortical neurons change dynamically, in response to artificial scotoma conditioning (Pettet & Gilbert, 1992) and to retinal lesions (Chino et al., 1992; Darian-Smith & Gilbert, 1995) in adult animals. The RF dynamics are of interest because they show how visual systems may adaptively overcome damage (from lesions, scotomas, or other failures), may enhance processing efficiency by altering RF coverage in response to visual demand, and may perform perceptual learning. This paper presents an afferent excitatory synaptic plasticity rule and a lateral inhibitory synaptic plasticity rule--the EXIN rules (Marshall, 1995)--to model persistent RF changes after artificial scotoma conditioning and retinal lesions. The EXIN model is compared to the LISSOM model (Sirosh et al., 1996) and to a neuronal adaptation model (Xing & Gerstein, 1994). The rules within each model are isolated and are analyzed independently, to elucidate their roles in adult cortical RF dynamics. Based on computer simulations, the EXIN lateral inhibitory synaptic plasticity rule and the LISSOM lateral excitatory synaptic plasticity rule produced the best fit with current neurophysiological data on visual cortical plasticity in adult animals (Chino et al., 1992; Pettet & Gilbert, 1992; Darian-Smith & Gilbert, 1995) including (1) the retinal position and shape of the expanding RFs; (2) the corticotopic direction in which responsiveness returns to the silenced cortex; (3) the direction of RF shifts; (4) the amount of change in response to blank stimuli; and (5) the lack of dynamic RF changes during conditioning with a retinal lesion in one eye and the unlesioned eye kept open, in adult animals. The effects of the LISSOM lateral inhibitory synaptic plasticity rule during artificial scotoma conditioning are in conflict with those of the other two LISSOM synaptic plasticity rules. A novel "complementary scotoma" conditioning experiment, in which stimulation of two complementary regions of visual space alternates repeatedly, is proposed to differentiate the predictions of the EXIN and LISSOM rules.

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Possible Roles of Spontaneous Waves and Dendritic Growth for Retinal Receptive Field Development

Cited by 12 publications

References 32 publications

The role of early neural activity in the maturation of turtle retinal function

The role of early neural activity in the maturation of turtle retinal function

Developmentally Regulated Spontaneous Activity in the Embryonic Chick Retina

Models of receptive-field dynamics in visual cortex

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