Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons

Salzberg, Brian M.; Grinvald, Amiram; Cohen, Lawrence B.; Davila, H. V.; Ross, W. N.

doi:10.1152/jn.1977.40.6.1281

Cited by 258 publications

(168 citation statements)

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“…Methods used for recording voltage-sensitive optical signals are similar to those described in detail elsewhere (Salzberg et al, 1977;Wu and Cohen, 1993;Keller et al, 1998). To wash out unbound dye, stained slices were perf used with AC SF for at least 15 min before initiating the optical recording.…”

Section: Methodsmentioning

confidence: 99%

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

2000

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We used optical imaging of voltage-sensitive dye signals to study the spatiotemporal spread of activity in the mouse barrel cortex, evoked by stimulation of thalamocortical afferents in an in vitro slice preparation. Stimulation of the thalamus, at low current intensity, results in activity largely restricted to a single barrel, and to the border between layers Vb and VI. Low concentrations of the GABA A receptor antagonist bicuculline increase the amplitude of the optical signals, without affecting their spatiotemporal propagation. Higher concentrations of bicuculline result in paroxysmal activity, which propagates via intracolumnar and intercolumnar excitatory pathways. Enhancing the activity of NMDA receptors, by removing Mg 2ϩ from the extracellular solution, dramatically alters the spatiotemporal pattern of excitation: activity spreads to supragranular and infragranular layers and adjacent barrel columns. This enhanced propagation is suppressed by the NMDA receptor antagonist AP5. A similar enhancement of activity propagation can be produced by stimulating the thalamus with a short, high-frequency pulse train. Application of AP5 suppresses the frequency-dependent spread of activity. These findings indicate that the spatiotemporal spread of activity in the barrel cortex is altered by varying the temporal patterns of thalamic inputs, via an NMDA receptor-mediated mechanism, and suggest that a similar process occurs during repetitive whisking activity. Key words: somatosensory cortex; voltage-sensitive dyes; glutamate; NMDA; GABA; epilepsy; temporal coding; mouseProcessing of sensory information in the cerebral cortex can be described as a hierarchical process, in which inputs from "specific" thalamic nuclei are integrated by their postsynaptic cortical targets, which, in turn, provide inputs to neurons in other layers of the same functional column and subsequently to adjacent columns (Gilbert, 1992;Keller, 1995;Rauschecker et al., 1997). Although this hierarchical scheme is oversimplified in that it omits factors such as parallel processing and feedback interactions, it is thought to faithfully represent at least the initial stages of cortical sensory processing (Stone et al., 1979;Felleman and Van Essen, 1991;Iwamura, 1993).To understand the mechanisms underlying cortical sensory processing, it is necessary to determine how thalamic inputs are integrated by their postsynaptic cortical neurons and propagated via intracolumnar and intercolumnar cortical pathways. This requires methods to identify discrete functional columns and to reveal the spatiotemporal propagation of thalamic inputs within and among these columns. In the present study we took advantage of a functional imaging approach (see Orbach and Cohen, 1983;Cinelli and Salzberg, 1987;Yuste et al., 1997;Keller et al., 1998) to investigate intracortical processing of thalamic inputs in the somatosensory cortex and its modulation by glutamatergic and GABAergic processes.The somatosensory cortex of certain rodent species contains representations of the my...

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Section: Methodsmentioning

confidence: 99%

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

2000

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“…Voltage-sensitive dyes are notorious for the photo-dynamic damage they produce in neuronal plasma membranes (Salzberg et al, 1977). Under some conditions, they are known to cause significant changes in membrane biophysical properties, such as action potential broadening (Antic et al, 1999).…”

Section: Are Basal Spikelets Artifacts Of Voltage-sensitive Dyes?mentioning

confidence: 99%

“…The advantages of optical recording of membrane potential changes over more traditional techniques were recognized long ago by Salzberg et al (1977). Some of these include: (1) recording from inaccessible membranes, (2) preservation of mechanical integrity of the plasma membrane, and (3) the capability of recording simultaneously from very many points in an image.…”

Section: Introductionmentioning

confidence: 99%

Initiation of Sodium Spikelets in Basal Dendrites of Neocortical Pyramidal Neurons

et al. 2005

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Cortical information processing relies critically on the processing of electrical signals in pyramidal neurons. Electrical transients mainly arise when excitatory synaptic inputs impinge upon distal dendritic regions. To study the dendritic aspect of synaptic integration one must record electrical signals in distal dendrites. Since thin dendritic branches, such as oblique and basal dendrites, do not support routine glass electrode measurements, we turned our effort towards voltage-sensitive dye recordings. Using the optical imaging approach we found and reported previously that basal dendrites of neocortical pyramidal neurons show an elaborate repertoire of electrical signals, including backpropagating action potentials and glutamate-evoked plateau potentials. Here we report a novel form of electrical signal, qualitatively and quantitatively different from backpropagating action potentials and dendritic plateau potentials. Strong glutamatergic stimulation of an individual basal dendrite is capable of triggering a fast spike, which precedes the dendritic plateau potential. The amplitude of the fast initial spikelet was actually smaller that the amplitude of the backpropagating action potential in the same dendritic segment. Therefore, the fast initial spike was dubbed "spikelet". Both the basal spikelet and plateau potential propagate decrementally towards the cell body, where they are reflected in the somatic whole-cell recordings. The low incidence of basal spikelets in the somatic intracellular recordings and the impact of basal spikelets on soma-axon action potential initiation are discussed.

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“…However, more recent evidence from both vertebrates and invertebrates has suggested that nervous systems may function in a distributed manner with many neurons involved in even simple behaviors and most neurons functioning in more than one behavior. Optical recordings using voltage-sensitive dyes can simultaneously monitor the action potential activity of many neurons (Salzberg et al, 1977;Grinvald et al, 198 1;Zecevic et al, 1989;Nakashima et al, 1992) and may thus be useful in discriminating between these two kinds of neuronal organization. The most complete recordings from the Aplysia abdominal ganglion can detect the spike activity of about 50% of the 900 neurons present in the ganglion (Coggeshall, 1967;Cash and Carew, 1989).…”

mentioning

confidence: 99%

Distributed aspects of the response to siphon touch in Aplysia: spread of stimulus information and cross-correlation analysis

Tsau

et al. 1994

J. Neurosci.

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We examined two aspects of the response to siphon stimulation in an attempt to test the hypothesis that the Aplysia CNS functions as a distributed system. First, we estimated the number of central neurons that respond to a light touch to the siphon skin. We made voltage- sensitive dye recordings from the abdominal, pleural, pedal, and cerebral ganglia. From these recordings we estimated that 220 abdominal neurons, 110 pleural neurons, and 650 pedal neurons were affected by the light touch. Thus, the information about this mild and localized stimulus is very widely distributed within the Aplysia CNS. This result allows the possibility that the Aplysia CNS functions as a distributed system. If only a small number of neurons had responded to the touch, it would have supported the conclusion that the gill-withdrawal reflex could be generated by a small, dedicated circuit. Second, we searched for correlations between the spike times of the individual abdominal ganglion neurons. Two time scales were examined: a millisecond time scale corresponding to the duration of a fast synaptic potential and a seconds time scale corresponding to the duration of the gill-withdrawal movement. Neuron pairs with highly correlated spike activity on a millisecond time scale must be connected by (or have a common input that uses) relatively powerful, fast, excitatory synapses. We expected that this kind of synaptic interaction would be relatively rare in nervous systems that functioned in a distributed manner. Indeed, only 0.3% of the neuron pairs had correlation coefficients of 0.15 or greater. These correlations accounted for approximately 2% of the action potentials generated in response to siphon stimulation. Thus, large, fast excitatory synaptic interactions appear to be relatively unimportant. This result is consistent with the hypothesis that the abdominal ganglion functions as a distributed system. When the longer time scale was used for the cross-correlograms, a large fraction of the cell pairs had correlated activity because many neurons are activated by the stimulus. It was not possible to interpret the slow correlations in terms of actual synaptic interactions between individual neurons. Our results are consistent with the possibility that the abdominal ganglion functions in a distributed manner. However, this evaluation is indirect and thus only tentative conclusions can be drawn. Evidence from several sources suggests that the neuronal interactions for generating the Aplysia gill-withdrawal reflex are complex.

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Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons

Abstract: 1. Using an optical method for measuring membrane potential, we have been able to monitor action-potential activity simultaneously in 14 neurons of the supraesophageal ganglion of the barnacle. 2. Under favorable conditions, 4-mV synaptic potentials could also be detected optically.

Cited by 258 publications

References 10 publications

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

Initiation of Sodium Spikelets in Basal Dendrites of Neocortical Pyramidal Neurons

Distributed aspects of the response to siphon touch in Aplysia: spread of stimulus information and cross-correlation analysis

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