The integrative properties of spiny distal dendrites.
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Biomedical subjects
J Midtgaard
Publications and source records attributed to J Midtgaard.
Membrane properties and synaptic responses of Golgi cells and stellate cells in the turtle cerebellum in vitro.
1. Intracellular recordings from anatomically identified Golgi cells and deep stellate cells were obtained in a slice preparation of the turtle cerebellar cortex. 2. Golgi cells and stellate cells had very similar firing patterns, which differed from those of Purkinje cells. In the interneurones, a short time constant and a high input resistance ensured a short response time. A pronounced spike after-hyperpolarization (spike AHP) participated in the rapid repolarization following a depolarizing input. The active and passive membrane properties of the interneurones ensured a very tight temporal coupling between input and output. 3. TTX abolished both the action potentials and a subthreshold depolarizing response. The Na+ excitability was increased by addition of Mn2+ or Co2+ to block calcium channels, or by addition of potassium channel blockers. 4. Ca2+ spikes and a Ca2+ plateau could be evoked following addition of potassium channel blockers. A partly 4-aminopyridine (4-AP)-sensitive transient hyperpolarization was found to control Ca2+ excitability in Golgi cells. It is suggested that this hyperpolarization is due to an A-like conductance. 5. A strong anomalous rectification was activated just below spike threshold, and dominated the subthreshold membrane potential at time scales longer than ca 100 ms. The anomalous rectification was partly blocked by Cs+. 6. Temporal integration over time scales up to ca 25 s was provided by activity-dependent adaptation in firing frequency and a long-lasting after-hyperpolarization (AHPL), which had both TTX-sensitive, Ca(2+)-independent, and Ca(2+)-dependent components. 7. Spontaneous IPSPs and EPSPs were abundant. The IPSPs were abolished by bicuculline. EPSPs were easily evoked by parallel fibre stimulation, had a shorter time course than in Purkinje cells, and were suppressed by the spike AHP. 8. Due to a short response time and a relatively short overall time frame for temporal integration, cerebellar interneurones operate on a faster time scale than the Purkinje cells, the output neurones of the cerebellar cortex. 9. It is suggested that information from shared sources, e.g. the parallel fibres, is distributed onto dynamically different cellular populations based on differences in the intrinsic membrane properties of the postsynaptic neurones.
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Stellate cell inhibition of Purkinje cells in the turtle cerebellum in vitro.
1. The stellate cell-mediated inhibition of Purkinje cells was studied by intracellular recordings in an in vitro slice preparation of the turtle cerebellar cortex. A graded inhibitory postsynaptic potential (IPSP) was recorded in Purkinje cells upon stimulation of the parallel fibre-stellate cell pathway. 2. The IPSP was abolished by bicuculline, and had a reversal potential around -75 mV, consistent with a GABAA receptor-operated Cl- conductance dominating the response investigated here. 3. Paired recordings from synaptically coupled stellate cells and Purkinje cells demonstrated that the inhibitory input from a single stellate cell is sufficient to reduce the firing in a Purkinje cell. 4. The extracellular-evoked IPSP interacted with the active postsynaptic membrane properties in the Purkinje cell. Interaction with both the Na+ plateau and the IA prolonged the responses to an IPSP, making the net effect of the inhibitory response dependent on the membrane potential in each postsynaptic neurone. 5. A precisely timed IPSP was particularly efficient in reducing dendritic Ca2+ influx. 6. The voltage-dependent Ca2+ component of a climbing fibre response (CFR) as well as of a parallel fibre (PF) input was reduced by the IPSP. 7. It is suggested that Ca2+ spike-mediated reduction in Purkinje cell excitability may be prevented by the stellate cell IPSP-mediated reduction in Ca2+ influx.
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Dendrite processing in more ways than one .
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Excitatory synaptic responses in turtle cerebellar Purkinje cells.
1. Climbing fibre responses (CFRs) and parallel fibre responses (PFRs) in Purkinje cells have been analysed in intracellular recordings obtained at various levels from cell body to terminal dendrites in the turtle cerebellum in vitro. 2. With increasing stimulus intensity, the PFR recorded in distal dendrites displayed an early regenerative component which was graded at rest and at hyperpolarized membrane potentials, but was all-or-none at depolarized membrane potentials. 3. The all-or-none component had the same characteristics as Ca2+ spikes triggered by passing depolarizing current through the recording electrode. 4. The repolarizing phase of the PFR had a fast component enhanced by depolarization and diminished by hyperpolarization. 5. In the mid-molecular layer the PFR also included a plateau component which was increasingly prolonged by depolarization and abolished by hyperpolarization. 6. CFRs recorded in the soma had a plateau component, prolonged by local depolarization and abolished by local hyperpolarization. 7. The CFR in distal dendrites included a regenerative component. In some cells this component appeared in an all-or-none manner with local depolarization. In other cells it was smoothly graded with local polarization. 8. In mid-molecular records the CFR was prolonged by local depolarization and presumably electrotonically affected by the configuration of the response more distally and proximally in the cell. 9. It is concluded that excitatory synaptic responses in Purkinje cells include a regenerative Ca2+-mediated spike component in the spiny dendrites and a plateau component located in the proximal dendrites and/or the cell body. It is shown that both responses are modulated in configuration by the local membrane potential. In the spiny dendrites activation and inactivation of the transient hyperpolarizing potential appear to govern the Ca2+ influx during the CFR.
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Synaptic control of excitability in turtle cerebellar Purkinje cells.
1. In turtle Purkinje cells in vitro successive climbing fibre responses (CFRs) gradually induced a hyperpolarization that persisted with maintained stimulation and decayed over minutes after climbing fibre stimulation was terminated. 2. The rate of development and the amplitude of this long-lasting hyperpolarization (LHP) increased with the frequency of CFRs. 3. The LHP was also induced by Ca2+ spikes evoked by current injection but not by Na+ spikes. The LHP was blocked by Co2+ but not by tetrodotoxin and could not be explained solely by an increased K+ conductance. 4. Depolarizing current during a train of CFRs enhanced the regenerative component of CFRs and promoted the LHP. Hyperpolarizing current during the stimulus train reduced the regenerative component of CFRs and attenuated the resulting LHP. 5. In the range of membrane potentials attained at different levels of climbing fibre activity the regenerative component of CFRs varied from being dominant at very low stimulus frequency (0.1 s-1) to being inconspicuous at high stimulus frequency (10 s-1). 6. It is concluded that successive CFRs induce a Ca2+-dependent, long-lasting hyperpolarization. The magnitude of the hyperpolarization is regulated by the rate of CFRs and by the voltage- and frequency-dependent configuration of each individual CFR. 7. The active, non-synaptic properties of turtle Purkinje cells make the Ca2+ influx during climbing fibre responses prone to regulation by on-going synaptic activity and by the after-effects of synaptic activity on a time scale of minutes. We suggest that this arrangement may enhance the capacity and complexity of spatial and temporal synaptic integration in Purkinje cells.
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Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro.
1. The intrinsic response properties of turtle Purkinje cells and the underlying conductances have been investigated with intradendritic and intrasomatic recordings in a slice preparation. 2. The active generation site for fast Na+ spikes was confined to the soma and for slow Ca2+ spikes to the dendrites. The configuration and generation of Ca2+ spikes was more affected by the level of extracellular K+ than were Na+ spikes. 3. Sodium spikes had a lower threshold than Ca2+ spikes at all recording sites. Sodium spike firing was abruptly initiated during depolarizing current pulses and the spike frequency increased from an early minimum to a higher steady-state level over a period of seconds or until the occurrence of Ca2+ spikes. Calcium spikes were always delayed by at least 100 ms from the onset of a depolarizing current pulse from rest. 4. The abrupt onset of Na+ spike firing was due to a tetrodotoxin-sensitive plateau potential. The phase of accelerating firing frequency and the delayed occurrence of Ca2+ spikes was due to a transient hyperpolarization activated by depolarization from rest or from more negative membrane potentials. The transient hyperpolarization was inactivated by depolarized holding potentials and was most probably generate by a rapidly inactivating K+ channel. 5. It is concluded that turtle Purkinje cells display the basic firing properties and underlying conductances known from Purkinje cells of other vertebrates. In turtle Purkinje cells Ca2+ spikes are actively generated in spiny dendrites and it is suggested that spiny dendrites rather than branch points are 'hot spots'. 6. The transient hyperpolarization, not previously described in Purkinje cells, seems particularly important for regulating Ca2+-dependent excitability.
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