The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell

Borg-Graham, Lyle J.

doi:10.1038/84007

Cited by 112 publications

(84 citation statements)

References 33 publications

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“…Conductance analysis methods were similar to those described by Borg-Graham (2001). It was assumed that the lightevoked synaptic inputs comprised two components: an excitatory component because of activation of nonselective cation channels having a reversal potential, V e ϭ 0 mV, and an inhibitory component with a reversal potential, V i , at the chloride equilibrium potential of approximately Ϫ65 mV.…”

Section: Methodsmentioning

confidence: 99%

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Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

2002

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The synaptic conductance of the On-Off direction-selective ganglion cells was measured during visual stimulation to determine whether the direction selectivity is a property of the circuitry presynaptic to the ganglion cells or is generated by postsynaptic interaction of excitatory and inhibitory inputs. Three synaptic asymmetries were identified that contribute to the generation of direction-selective responses: (1) a presynaptic mechanism producing stronger excitation in the preferred direction, (2) a presynaptic mechanism producing stronger inhibition in the opposite direction, and (3) postsynaptic interaction of excitation with spatially offset inhibition. Although the on-and off-responses showed the same directional tuning, the off-response was generated by all three mechanisms, whereas the on-response was generated primarily by the two presynaptic mechanisms. The results indicate that, within a single neuron, different strategies are used within distinct dendritic arbors to accomplish the same neural computation.Key words: direction selectivity; ganglion cells; synaptic conductance; inhibition; excitation; dendritic integration; on-and off-pathways; rabbit retinaThe direction-selective ganglion cells (DSGCs) in the rabbit retina are a model system for investigating neural computation (Vaney et al., 2001). These cells respond strongly to an image moving in a preferred direction but only weakly to an image moving in the opposite "null" direction. The foundation for understanding the cellular mechanisms of direction selectivity in vertebrates was laid by Barlow and Levick (1965), whose extracellular recordings from DSGCs indicated that direction selectivity was mediated primarily by inhibition activated by nulldirection image motion. Strong support for the inhibitory model was provided by subsequent pharmacological experiments, which showed that GABA A -receptor antagonists abolish direction selectivity (Wyatt and Daw, 1976;Ariel and Daw, 1982;Kittila and Massey, 1997). However, these extracellular recording experiments provided no information about whether the inhibition acted directly on the DSGC or presynaptically on the excitatory interneurons.Torre and Poggio (1978) proposed a postsynaptic model in which DSGCs receive an inhibitory input that is spatially offset relative to the excitatory input; moreover, the inhibition is nondirectional, being activated equally well by image motion in the preferred and null directions. During null-direction motion, the spatial offset means that delayed inhibitory synapses at locations ahead of the stimulus are activated and veto the excitation as the stimulus sweeps across the receptive field. For preferreddirection motion, the inhibition trails behind the stimulus and thus arrives too late to veto the excitation. For this model to work, the inhibition must act locally within the dendritic arbor of the DSGC. This occurs when the inhibitory reversal potential is at, or close to, the resting potential of the cell, and therefore the inhibitory input does not polarize the c...

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Section: Methodsmentioning

confidence: 99%

“…To separate the conductance records into excitatory and inhibitory components, we assumed that the DSGCs were isopotential (Anderson et al, 2000;Borg-Graham, 2001). However, a simple test confirmed the expectation that this is an approximation.…”

Section: Errors In Conductance Estimates In a Non-isopotential Neuronmentioning

confidence: 99%

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

2002

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“…We failed to obtain confident estimates of Gexc(t) and Ginh(t) using methods described previously (Borg-Graham, 2001). The reason for that derived from the need to place constraints to solve algebraic equations, which substantially distorted results.…”

Section: Methodsmentioning

confidence: 99%

Synaptic Contributions to Focal and Widespread Spatiotemporal Dynamics in the Isolated Rat SubiculumIn Vitro

Prida¹,

Gal²

2004

J. Neurosci.

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The subiculum, which has a strategic position in controlling hippocampal activity, is receiving significant attention in epilepsy research. However, the functional organization of subicular circuits remains unknown. Here, we combined different recording and analytical methods to study focal and widespread population activity in the isolated subiculum in zero Mg 2ϩ media. Patch and field recordings were combined to examine the contribution of different cell types to population activity. The properties of cells leading field activity were examined. Predictive factors for a cell to behave as leader included exhibiting the bursting phenotype, displaying a low firing threshold, and having more distal apical dendrites. A subset of bursting cells constituted the first glutamatergic type that led a recruitment process that subsequently activated additional excitatory as well as inhibitory cells. This defined a sequence of synaptic excitation and inhibition that was studied by measuring the associated conductance changes and the evolution of the composite reversal potential. It is shown that inhibition was time-locked to excitation, which shunted excitatory inputs and suppressed firing during focal activity. This was recorded extracellularly as a multi-unit ensemble of active cells, the spatial boundaries of which were controlled by inhibition in contrast to widespread epileptiform activity. Focal activity was not dependent on the preparation or the developmental state because it was also recorded under 5 mM [K ϩ ] o and in adult tissue. Our data indicate that the subicular networks can be spontaneously organized as leader-follower local circuits in which excitation is mainly driven by a subset of bursting cells and inhibition controls spatiotemporal firing.

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“…Among the most intuitive examples of how time delays are used in neural computations are models of sound localization (Knudsen & Konishi 1979) and direction selectivity in motion perception (Borg-Graham 2001). We suggest that the biophysical principles that establish the circuitry and mechanisms for time delays are also responsible for mechanisms that compensate for the delays, thus assuaging harmful effects of delays.…”

Section: Neural Prediction and Forward Shiftsmentioning

confidence: 99%

Compensating time delays with neural predictions: are predictions sensory or motor?

Nijhawan

2009

Phil. Trans. R. Soc. A.

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Neural delays are a general property of computations carried out by neural circuits. Delays are a natural consequence of temporal summation and coding used by the nervous system to integrate information from multiple resources. For adaptive behaviour, however, these delays must be compensated. In order to sense and interact with moving objects, for example, the visual system must predict the future position of the object to compensate for delays. In this paper, we address two critical questions concerning the implementation of the compensation mechanisms in the brain, namely, where does compensation occur and how is it realized. We present evidence showing that compensation can happen in both the motor and sensory systems, and that compensation using 'diagonal neural pathways' is a suitable strategy for implementing compensation in the visual system. In this strategy, neural signals in the early stage of information processing are sent to the future cortical positions that correspond to the distance the object will travel in the period of transmission delay. We propose a computational model to elucidate this using the retinal visual information pathway.

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The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell

Cited by 112 publications

References 33 publications

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

Synaptic Contributions to Focal and Widespread Spatiotemporal Dynamics in the Isolated Rat SubiculumIn Vitro

Compensating time delays with neural predictions: are predictions sensory or motor?

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