Characterisation of rat superficial superior colliculus neurones: firing properties and sensitivity to GABA

Michelle Diane Edwards, A. M. White, Bettina Platt

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Physiological, pharmacological and morphological properties of superficial superior coiliculus neurones (n=93) were characterised using whole-cell patch-clamp recordings in rat brain slices. Six cell types (narrow- and wide-field vertical, horizontal, piriform, marginal and stellate) were identified based on Lucifer Yellow labelling but no cell type-specific spike pattern could be identified. Resting membrane potentials were homogeneous (mean: -67.1+/-0.7 mV, n=48), and spike frequencies ranged from 10 to 70 Hz (80 pA current injection). About 66% of the cells displayed regular and sustained spike production, throughout all neuronal categories. Rebound spikes and spontaneous activity were observed frequently in all cell types. Synaptically evoked action potentials appeared as single spikes (mean amplitude: 76.0+/-3.2 mV, n=34) followed by a fast after-hyperpolarising potential (mean amplitude: 25.4+/-1.4 mV, n=34) and variable late potentials (late after-depolarising and/or -hyperpolarising).

Pharmacologically, a characterisation using GABA and its subtype-specific agonists indicated a strong inhibitory influence of this transmitter system on >90% of cells. The GABA(A) receptor agonist, 4,5,6,7-tetrahydroisoxazolo[5,4c]pyridin-3-ol (100 muM), caused a reversible hyperpolarisation (similar to9 mV) and spike inhibition of all neurones studied. This was more pronounced for intrinsic than for synaptically evoked spikes. Assessment of the GABA(C) receptor agonist, cis-4-aminocrotonic acid (I mM), also revealed a hyperpolarisation (similar to3 mV) and an inhibitory action on firing, but this was not as potent and homogeneous, compared to the GABA(A) receptor agonist. Further, the GABA(B) receptor agonist, baclofen (50-100 muM), had more variable (hyperpolarising, depolarising or no change) effects on the membrane potential. It showed little modulation of current-induced action potentials but fully blocked synaptic spikes.

Assessment of GABA receptor antagonist actions revealed the presence of weak tonic and strong phasic GABA(A) receptor-mediated inhibition in the superficial superior colliculus: application of the GABA(A) receptor antagonist, bicuculline (100 muM), led to a generally enhanced excitability and depolarisation (similar to5 mV). Intrinsic firing was somewhat enhanced, but synaptic spiking was drastically potentiated and prolonged. In contrast, 1,2,5,6-tetrahydro-(pyridin-4-yl) methylphosphinic acid (TPMPA; 100 muM), the GABA(C) receptor antagonist, produced little effect on these physiological parameters. The GABA(B) receptor antagonist, CGP35348 (200 muM), caused a partial inhibition of late after-hyperpolarising potentials (similar to30%).

Uptake of GABA contributes little to endogenous inhibition in the superior colliculus slice preparation, as suggested by the action of GABA uptake inhibitors SKF89976 (50-100 muM) and nipecotic acid (200-500 muM), both had no obvious effect on physiological parameters. However, in the presence of these compounds, sub-maximal inhibitory actions of GABA were potentiated.

In conclusion, different cell types in the superficial superior colliculus do not display distinct physiological properties and are subject to strong inhibitory modulation. We therefore suggest that signal processing in this brain region does not require cell type-specific encoding of information. In line with evidence provided by previous in vivo investigations, identification of visual stimuli and orientation responses appears to be realised via the network properties of the receptive fields that form topographic maps. (C) 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.

Original languageEnglish
Pages (from-to)93-104
Number of pages11
JournalNeuroscience
Volume110
Issue number1
DOIs
Publication statusPublished - 2002

Keywords

  • GABA receptors
  • midbrain
  • morphology
  • patch clamp
  • visual system
  • CENTRAL-NERVOUS-SYSTEM
  • RECEPTOR RHO-SUBUNIT
  • INTERLAMINAR CONNECTIONS
  • OPTIC LAYER
  • TREE SHREW
  • ORGANIZATION
  • BRAIN
  • CAT
  • PROJECTIONS
  • EXPRESSION

Cite this

Characterisation of rat superficial superior colliculus neurones: firing properties and sensitivity to GABA. / Edwards, Michelle Diane; White, A. M.; Platt, Bettina.

In: Neuroscience, Vol. 110, No. 1, 2002, p. 93-104.

Research output: Contribution to journalArticle

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title = "Characterisation of rat superficial superior colliculus neurones: firing properties and sensitivity to GABA",
abstract = "Physiological, pharmacological and morphological properties of superficial superior coiliculus neurones (n=93) were characterised using whole-cell patch-clamp recordings in rat brain slices. Six cell types (narrow- and wide-field vertical, horizontal, piriform, marginal and stellate) were identified based on Lucifer Yellow labelling but no cell type-specific spike pattern could be identified. Resting membrane potentials were homogeneous (mean: -67.1+/-0.7 mV, n=48), and spike frequencies ranged from 10 to 70 Hz (80 pA current injection). About 66{\%} of the cells displayed regular and sustained spike production, throughout all neuronal categories. Rebound spikes and spontaneous activity were observed frequently in all cell types. Synaptically evoked action potentials appeared as single spikes (mean amplitude: 76.0+/-3.2 mV, n=34) followed by a fast after-hyperpolarising potential (mean amplitude: 25.4+/-1.4 mV, n=34) and variable late potentials (late after-depolarising and/or -hyperpolarising).Pharmacologically, a characterisation using GABA and its subtype-specific agonists indicated a strong inhibitory influence of this transmitter system on >90{\%} of cells. The GABA(A) receptor agonist, 4,5,6,7-tetrahydroisoxazolo[5,4c]pyridin-3-ol (100 muM), caused a reversible hyperpolarisation (similar to9 mV) and spike inhibition of all neurones studied. This was more pronounced for intrinsic than for synaptically evoked spikes. Assessment of the GABA(C) receptor agonist, cis-4-aminocrotonic acid (I mM), also revealed a hyperpolarisation (similar to3 mV) and an inhibitory action on firing, but this was not as potent and homogeneous, compared to the GABA(A) receptor agonist. Further, the GABA(B) receptor agonist, baclofen (50-100 muM), had more variable (hyperpolarising, depolarising or no change) effects on the membrane potential. It showed little modulation of current-induced action potentials but fully blocked synaptic spikes.Assessment of GABA receptor antagonist actions revealed the presence of weak tonic and strong phasic GABA(A) receptor-mediated inhibition in the superficial superior colliculus: application of the GABA(A) receptor antagonist, bicuculline (100 muM), led to a generally enhanced excitability and depolarisation (similar to5 mV). Intrinsic firing was somewhat enhanced, but synaptic spiking was drastically potentiated and prolonged. In contrast, 1,2,5,6-tetrahydro-(pyridin-4-yl) methylphosphinic acid (TPMPA; 100 muM), the GABA(C) receptor antagonist, produced little effect on these physiological parameters. The GABA(B) receptor antagonist, CGP35348 (200 muM), caused a partial inhibition of late after-hyperpolarising potentials (similar to30{\%}).Uptake of GABA contributes little to endogenous inhibition in the superior colliculus slice preparation, as suggested by the action of GABA uptake inhibitors SKF89976 (50-100 muM) and nipecotic acid (200-500 muM), both had no obvious effect on physiological parameters. However, in the presence of these compounds, sub-maximal inhibitory actions of GABA were potentiated.In conclusion, different cell types in the superficial superior colliculus do not display distinct physiological properties and are subject to strong inhibitory modulation. We therefore suggest that signal processing in this brain region does not require cell type-specific encoding of information. In line with evidence provided by previous in vivo investigations, identification of visual stimuli and orientation responses appears to be realised via the network properties of the receptive fields that form topographic maps. (C) 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.",
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T1 - Characterisation of rat superficial superior colliculus neurones: firing properties and sensitivity to GABA

AU - Edwards, Michelle Diane

AU - White, A. M.

AU - Platt, Bettina

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N2 - Physiological, pharmacological and morphological properties of superficial superior coiliculus neurones (n=93) were characterised using whole-cell patch-clamp recordings in rat brain slices. Six cell types (narrow- and wide-field vertical, horizontal, piriform, marginal and stellate) were identified based on Lucifer Yellow labelling but no cell type-specific spike pattern could be identified. Resting membrane potentials were homogeneous (mean: -67.1+/-0.7 mV, n=48), and spike frequencies ranged from 10 to 70 Hz (80 pA current injection). About 66% of the cells displayed regular and sustained spike production, throughout all neuronal categories. Rebound spikes and spontaneous activity were observed frequently in all cell types. Synaptically evoked action potentials appeared as single spikes (mean amplitude: 76.0+/-3.2 mV, n=34) followed by a fast after-hyperpolarising potential (mean amplitude: 25.4+/-1.4 mV, n=34) and variable late potentials (late after-depolarising and/or -hyperpolarising).Pharmacologically, a characterisation using GABA and its subtype-specific agonists indicated a strong inhibitory influence of this transmitter system on >90% of cells. The GABA(A) receptor agonist, 4,5,6,7-tetrahydroisoxazolo[5,4c]pyridin-3-ol (100 muM), caused a reversible hyperpolarisation (similar to9 mV) and spike inhibition of all neurones studied. This was more pronounced for intrinsic than for synaptically evoked spikes. Assessment of the GABA(C) receptor agonist, cis-4-aminocrotonic acid (I mM), also revealed a hyperpolarisation (similar to3 mV) and an inhibitory action on firing, but this was not as potent and homogeneous, compared to the GABA(A) receptor agonist. Further, the GABA(B) receptor agonist, baclofen (50-100 muM), had more variable (hyperpolarising, depolarising or no change) effects on the membrane potential. It showed little modulation of current-induced action potentials but fully blocked synaptic spikes.Assessment of GABA receptor antagonist actions revealed the presence of weak tonic and strong phasic GABA(A) receptor-mediated inhibition in the superficial superior colliculus: application of the GABA(A) receptor antagonist, bicuculline (100 muM), led to a generally enhanced excitability and depolarisation (similar to5 mV). Intrinsic firing was somewhat enhanced, but synaptic spiking was drastically potentiated and prolonged. In contrast, 1,2,5,6-tetrahydro-(pyridin-4-yl) methylphosphinic acid (TPMPA; 100 muM), the GABA(C) receptor antagonist, produced little effect on these physiological parameters. The GABA(B) receptor antagonist, CGP35348 (200 muM), caused a partial inhibition of late after-hyperpolarising potentials (similar to30%).Uptake of GABA contributes little to endogenous inhibition in the superior colliculus slice preparation, as suggested by the action of GABA uptake inhibitors SKF89976 (50-100 muM) and nipecotic acid (200-500 muM), both had no obvious effect on physiological parameters. However, in the presence of these compounds, sub-maximal inhibitory actions of GABA were potentiated.In conclusion, different cell types in the superficial superior colliculus do not display distinct physiological properties and are subject to strong inhibitory modulation. We therefore suggest that signal processing in this brain region does not require cell type-specific encoding of information. In line with evidence provided by previous in vivo investigations, identification of visual stimuli and orientation responses appears to be realised via the network properties of the receptive fields that form topographic maps. (C) 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.

AB - Physiological, pharmacological and morphological properties of superficial superior coiliculus neurones (n=93) were characterised using whole-cell patch-clamp recordings in rat brain slices. Six cell types (narrow- and wide-field vertical, horizontal, piriform, marginal and stellate) were identified based on Lucifer Yellow labelling but no cell type-specific spike pattern could be identified. Resting membrane potentials were homogeneous (mean: -67.1+/-0.7 mV, n=48), and spike frequencies ranged from 10 to 70 Hz (80 pA current injection). About 66% of the cells displayed regular and sustained spike production, throughout all neuronal categories. Rebound spikes and spontaneous activity were observed frequently in all cell types. Synaptically evoked action potentials appeared as single spikes (mean amplitude: 76.0+/-3.2 mV, n=34) followed by a fast after-hyperpolarising potential (mean amplitude: 25.4+/-1.4 mV, n=34) and variable late potentials (late after-depolarising and/or -hyperpolarising).Pharmacologically, a characterisation using GABA and its subtype-specific agonists indicated a strong inhibitory influence of this transmitter system on >90% of cells. The GABA(A) receptor agonist, 4,5,6,7-tetrahydroisoxazolo[5,4c]pyridin-3-ol (100 muM), caused a reversible hyperpolarisation (similar to9 mV) and spike inhibition of all neurones studied. This was more pronounced for intrinsic than for synaptically evoked spikes. Assessment of the GABA(C) receptor agonist, cis-4-aminocrotonic acid (I mM), also revealed a hyperpolarisation (similar to3 mV) and an inhibitory action on firing, but this was not as potent and homogeneous, compared to the GABA(A) receptor agonist. Further, the GABA(B) receptor agonist, baclofen (50-100 muM), had more variable (hyperpolarising, depolarising or no change) effects on the membrane potential. It showed little modulation of current-induced action potentials but fully blocked synaptic spikes.Assessment of GABA receptor antagonist actions revealed the presence of weak tonic and strong phasic GABA(A) receptor-mediated inhibition in the superficial superior colliculus: application of the GABA(A) receptor antagonist, bicuculline (100 muM), led to a generally enhanced excitability and depolarisation (similar to5 mV). Intrinsic firing was somewhat enhanced, but synaptic spiking was drastically potentiated and prolonged. In contrast, 1,2,5,6-tetrahydro-(pyridin-4-yl) methylphosphinic acid (TPMPA; 100 muM), the GABA(C) receptor antagonist, produced little effect on these physiological parameters. The GABA(B) receptor antagonist, CGP35348 (200 muM), caused a partial inhibition of late after-hyperpolarising potentials (similar to30%).Uptake of GABA contributes little to endogenous inhibition in the superior colliculus slice preparation, as suggested by the action of GABA uptake inhibitors SKF89976 (50-100 muM) and nipecotic acid (200-500 muM), both had no obvious effect on physiological parameters. However, in the presence of these compounds, sub-maximal inhibitory actions of GABA were potentiated.In conclusion, different cell types in the superficial superior colliculus do not display distinct physiological properties and are subject to strong inhibitory modulation. We therefore suggest that signal processing in this brain region does not require cell type-specific encoding of information. In line with evidence provided by previous in vivo investigations, identification of visual stimuli and orientation responses appears to be realised via the network properties of the receptive fields that form topographic maps. (C) 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.

KW - GABA receptors

KW - midbrain

KW - morphology

KW - patch clamp

KW - visual system

KW - CENTRAL-NERVOUS-SYSTEM

KW - RECEPTOR RHO-SUBUNIT

KW - INTERLAMINAR CONNECTIONS

KW - OPTIC LAYER

KW - TREE SHREW

KW - ORGANIZATION

KW - BRAIN

KW - CAT

KW - PROJECTIONS

KW - EXPRESSION

U2 - 10.1016/S0306-4522(01)00558-9

DO - 10.1016/S0306-4522(01)00558-9

M3 - Article

VL - 110

SP - 93

EP - 104

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

IS - 1

ER -