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Specific Systems of the Reticular Core: Serotonin

G. K. Aghajanian, C. P. Vandermaelen

10.1002/cphy.cp010404

Source: Supplement 4: Handbook of Physiology, The Nervous System, Intrinsic Regulatory Systems of the Brain

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Regulation of Serotonergic Neurons
1.1 Intrinsic Regulation
1.2 γ‐Aminobutyric Acid and Substance P Inputs to Serotonergic Neurons
1.3 Noradrenergic Input to Serotonergic Neurons
2 Postsynaptic Actions of Serotonin
2.1 Serotonergic Inhibition
2.2 Serotonergic Excitation and Facilitation
3 Summary
3.1 Regulation of Serotonergic Neurons
3.2 Postsynaptic Actions of Serotonin
3.3 Speculations on Function of Serotonin
Figure 1. Figure 1.

Intracellular recording in vivo of spontaneous activity of rat dorsal raphe neuron with typical slow, regular firing pattern. Rate of this cell's firing was ∼1.7 spikes/s. Note large postspike afterhyperpolarization and gradual interspike depolarization.

From Aghajanian and VanderMaelen 7
Figure 2. Figure 2.

A: postactivation hyperpolarization of dorsal raphe neuron induced by intracellular depolarizing pulses. Top trace, spontaneous spike in absence of depolarizing pulse. Middle trace, burst of 4 spikes induced by 0.5‐nA depolarizing pulse. Note afterhyperpolarization after cessation of depolarizing pulse, and reduced voltage deflection produced by 0.5‐nA hyperpolarizing pulse in postactivation period. Bottom trace, similar to middle trace, except 1.0‐nA depolarizing pulse was used. Current monitor is displayed beneath membrane potential traces. Intracellular injections of current were made through recording electrode by means of balanced bridge circuit. Data were stored on FM tape recorder and retrieved with storage oscilloscope. B: poststimulus‐time histograms showing postactivation suppression of firing in same cell as in A. Top trace, 36 spikes accumulated randomly after 10 sweeps during 2‐s sampling intervals (no depolarizing pulse). Middle trace, 10 presentations of 0.5‐nA depolarizing pulse (0.2 Hz) evoked total of 38 spikes ( = 3.8 spikes/pulse); poststimulus period of total inhibition lasts nearly 0.5 s. Bottom trace, 10 presentations of 1.0‐nA depolarizing pulse evoked 76 spikes ( = 7.6 spikes/pulse); poststimulus inhibition lasts nearly 1.0 s.

From Aghajanian and VanderMaelen 7
Figure 3. Figure 3.

Simultaneous recording from serotonergic dorsal raphe neuron showing effects of lysergic acid diethylamide (LSD) on membrane potential (A), firing rate (B), and neuronal input resistance (C). A: low‐pass filtered DC trace showing hyperpolarization of dorsal raphe neuron after injection of LSD (50 μg/kg body wt, ip). Thickness of initial portion of trace reflects slow interspike fluctuations in membrane potential. After injection of LSD, membrane potential no longer fluctuates markedly and remains at 4–6 mV below highest excursions prior to injection. B: average‐rate record (*) showing gradual inhibition of firing of same cell as in A after injection of LSD. Counter resets to 0 every 10 s, giving rate in spikes/10 s. C: input resistance (Rinput) decreases slightly after injection of LSD. Resistance values were calculated by Ohm's law, with isolated voltage deflections induced by periodic constant‐current hyperpolarizing pulses (0.2 nA, 0.2 Hz). D: top trace, spontaneous spikes prior to injection of LSD taken from point shown on average‐rate record (*). Bottom trace, last spontaneous firing of this cell before complete inhibition by LSD; taken from point shown on average‐rate record (**). Usual interspike depolarization does not occur after this spike.

From Aghajanian and VanderMaelen 7
Figure 4. Figure 4.

Frontal section through midbrain showing dorsal raphe neuron labeled with horseradish peroxidase. Enzyme was ejected into cell with depolarizing pulses (4 nA, 1 Hz, 900‐ms duration) applied for 4 min. Note polygonal or multipolar structure; somatic and dendritic spines were visible at higher magnifications. MLF, medial longitudinal fasciculus. Vibratone sections (100 μm) with cresyl violet acetate counterstain. Bars = 50 μm.

From Aghajanian and VanderMaelen 7
Figure 5. Figure 5.

Inhibitory responses of guinea pig hippocampal CA1 neurons to serotonin (5‐HT), recorded intracellularly. A: electrode positioned in CA1 region. ALV, alveus; OR, stratum oriens; PYR, stratum pyramidale; RAD, stratum radiatum; L‐M, stratum lacunosum‐moleculare; REC, recording electrode; 5‐HT, iontophoresis electrode; and STIM, stimulating electrode. B: membrane potential of neuron before (a), during (b), and after (c) iontophoresis with 5‐HT HCI (20 nA). Cell is hyperpolarized during 5‐HT iontophoresis. Membrane potential recordings are low‐pass filtered at 2 Hz during reproduction from tape recorder. C: cell input resistance before (a), during (b), and after (c) application of 5‐HT, measured with hyperpolarizing current pulses of 1 nA. Input resistance was decreased during 5‐HT application. D: same type of response as in C, but elicited with diffusion from glass pipette containing 10−3 M 5‐HT creatine sulfate. E: example of unbalanced (a) and balanced (b) recording electrode resistance.

From Jahnsen 77
Figure 6. Figure 6.

Effects of 5‐HT on inhibitory postsynaptic potential (IPSP). Intracellular recordings from rat hippocampus CA1 pyramidal neurons in vitro. A: specimen record of cellular membrane responses to 5‐HT applied by microdroplet at time indicated by arrow. Marked hyperpolarization associated with decrease in input resistance was recorded. Input resistance was measured by injecting constant‐current hyperpolarizing pulses. B: IPSP was produced by stimulation (arrow) near pyramidal layer. Inhibitory stimuli were applied simultaneously with series of hyperpolarizing current pulses (nA shown) to measure IPSP reversal potential (−68 mV). C: same as B, but after 5‐HT application. Membrane potential was slightly below IPSP reversal potential, and no IPSP was seen. An IPSP could still be produced by applying stimulation on top of depolarizing current pulse (+0.4 nA). D: current‐voltage plot of cell's responses to series of hyperpolarizing pulses, before and after 5‐HT application. Reversal potential for 5‐HT is ca. −83 mV. E: magnitude of IPSP at various potential levels before and after 5‐HT application (symbols as in D), indicating IPSP reversal potential that is not changed by 5‐HT.

From Segal 129
Figure 7. Figure 7.

Effect of extracellular K+ on membrane potential and resistance responses to 5‐HT applied by microdroplet (arrows). A: response to 5‐HT in normal (5 mM) K+ medium. B: same cell, after superfusion with 10 mM K+. Note change in potential (+10 mV) and smaller change in potential produced by 5‐HT. C: same cell, superfused with 10 mM K+ and hyperpolarized with continuous current. 5‐HT no longer produced hyperpolarization, although resistance change is evident.

From Segal 129
Figure 8. Figure 8.

Facilitation of glutamate‐induced excitation of rat facial motoneurons by 5‐HT. Singleunit activity was recorded extracellularly, and substances were applied by microiontophoresis. Ratemeter recordings in A, B, and C show number of spikes occurring in each 10‐s period. A: 5‐HT (10 nA) reduced threshold required for glutamate‐induced activation of unit. 5‐HT (200 nA) failed to directly excite neuron. B: facilitating effect of 1‐min pulses of 5‐HT on glutamate‐induced excitation (G, 2 nA) of motoneuron. C: facilitation of subthreshold excitatory effect of glutamate (G, 7 nA) by 5‐HT. D: cumulative dose‐response curve for glutamate‐induced excitation of rat facial motoneurons in presence (left) and absence (right) of 5‐HT (10 nA). Abscissa, duration of glutamate ejection. Ordinate, percentage of cells showing maximal excitation (overdepolarization) at given duration of glutamate ejection.

From McCall and Aghajanian 94
Figure 9. Figure 9.

Facilitation of glutamate‐evoked excitation of a rat spinal motoneuron by 5‐HT and norepinephrine (NA). Single‐unit activity was recorded extracellularly, and substances were applied by microiontophoresis. Height of bars indicates number of spikes fired during short application of glutamate, which was given repeatedly. Cells did not fire spontaneously in absence of glutamate. A: pre‐metergoline. 5‐HT and NA facilitation of glutamate‐evoked activity in this motoneuron was preceded by brief periods of inhibition during current application, specified in nA. B: post‐metergoline (1 mg/kg body wt, iv). Metergoline reduced glutamate‐evoked activity and prevented 5‐HT increase, but not NA increase, of evoked activity. C: recovery. Glutamate sensitivity recovered eventually, along with response to 5‐HT.

From White and Neuman 154
Figure 10. Figure 10.

Typical response of rat facial motoneuron (recorded intracellularly) to iontophoretically applied 5‐HT. Simultaneous pen recordings of resting membrane potential (A), neuronal input resistance (B), and number of spikes occurring during intracellularly injected depolarizing current pulse (C), which is measure of neuron excitability. A: resting membrane potential, with electrotonic displacements of membrane potential and spike potentials filtered out. B: amplitude of voltage displacements in response to 2.0‐nA hyperpolarizing pulses, with scale on right adjusted according to Ohm's law to give input resistance in MΩ. Bar between A and B indicates duration and ejection current of iontophoretically applied 5‐HT. C: output of spike counter, which was reset after each depolarizing pulse. All spikes were triggered by intracellular depolarizing current pulse, which occurred once every 2 s, and which was adjusted to 67% of threshold to fire 1 spike before 5‐HT was applied. D: oscilloscope traces (1–4) occurred at times indicated by arrows in A. Current monitor trace is shown at top. Time marker occurred once every 10 s, and applies to A‐C. Distance between iontophoretic and recording electrode tips was ∼45 μm. 5‐HT caused membrane depolarization, increased input resistance (Rinput) and excitability.

From VanderMaelen and Aghajanian, unpublished observations
Figure 11. Figure 11.

Responses of rat facial motoneuron to iontophoretically applied glycine (GLY), γ‐aminobutyric acid (GABA), and 5‐HT. A, B, and C: simultaneous pen recordings, as described in Fig. 10. Durations and amplitudes (in nA) of iontophoretic currents are indicated by bars below A. Membrane responses to GLY and GABA were depolarizing due to Cl− diffusion into cell from recording electrode, which contained 3 M KCI. Selected sweeps of oscilloscope are shown above A and occurred at times indicated by arrows. Current monitor trace is above each voltage‐recording trace. B: longer and shorter lines were caused by alternating 1.0‐ and 2.0‐nA hyperpolarizing current pulses, 1 pulse/s. Scale to right in B is for larger (2.0 nA) pulses only. No depolarizing current pulses were injected. Spike activity was spontaneous (i.e., not evoked by depolarizing current pulses). This experiment indicates that 5‐HT response is not due to decrease in membrane conductance of Cl−.

From VanderMaelen and Aghajanian 143
Figure 12. Figure 12.

Effects of depolarizing and hyperpolarizing current injections on membrane potential responses of rat facial motoneuron to iontophoretically applied 5‐HT and excitatory amino acid DL‐homocysteic acid (DLH). In each case DLH was ejected at 40 nA for 20 s, and 5‐HT was ejected at 154 nA for 50 s. Cell membrane was continuously depolarized or hyperpolarized by injection of current; amplitude of current is shown (in nA) to right of each trace. C: control responses when no current was injected into neuron. Resting potential in control condition was −72 mV and antidromic spike amplitude (not shown) was 92 mV. Time and voltage calibrations in A also apply to B‐E. Hyperpolarizing neuron by current injection abolished response to 5‐HT but had little effect on response to DLH.

From VanderMaelen and Aghajanian 143


Figure 1.

Intracellular recording in vivo of spontaneous activity of rat dorsal raphe neuron with typical slow, regular firing pattern. Rate of this cell's firing was ∼1.7 spikes/s. Note large postspike afterhyperpolarization and gradual interspike depolarization.

From Aghajanian and VanderMaelen 7


Figure 2.

A: postactivation hyperpolarization of dorsal raphe neuron induced by intracellular depolarizing pulses. Top trace, spontaneous spike in absence of depolarizing pulse. Middle trace, burst of 4 spikes induced by 0.5‐nA depolarizing pulse. Note afterhyperpolarization after cessation of depolarizing pulse, and reduced voltage deflection produced by 0.5‐nA hyperpolarizing pulse in postactivation period. Bottom trace, similar to middle trace, except 1.0‐nA depolarizing pulse was used. Current monitor is displayed beneath membrane potential traces. Intracellular injections of current were made through recording electrode by means of balanced bridge circuit. Data were stored on FM tape recorder and retrieved with storage oscilloscope. B: poststimulus‐time histograms showing postactivation suppression of firing in same cell as in A. Top trace, 36 spikes accumulated randomly after 10 sweeps during 2‐s sampling intervals (no depolarizing pulse). Middle trace, 10 presentations of 0.5‐nA depolarizing pulse (0.2 Hz) evoked total of 38 spikes ( = 3.8 spikes/pulse); poststimulus period of total inhibition lasts nearly 0.5 s. Bottom trace, 10 presentations of 1.0‐nA depolarizing pulse evoked 76 spikes ( = 7.6 spikes/pulse); poststimulus inhibition lasts nearly 1.0 s.

From Aghajanian and VanderMaelen 7


Figure 3.

Simultaneous recording from serotonergic dorsal raphe neuron showing effects of lysergic acid diethylamide (LSD) on membrane potential (A), firing rate (B), and neuronal input resistance (C). A: low‐pass filtered DC trace showing hyperpolarization of dorsal raphe neuron after injection of LSD (50 μg/kg body wt, ip). Thickness of initial portion of trace reflects slow interspike fluctuations in membrane potential. After injection of LSD, membrane potential no longer fluctuates markedly and remains at 4–6 mV below highest excursions prior to injection. B: average‐rate record (*) showing gradual inhibition of firing of same cell as in A after injection of LSD. Counter resets to 0 every 10 s, giving rate in spikes/10 s. C: input resistance (Rinput) decreases slightly after injection of LSD. Resistance values were calculated by Ohm's law, with isolated voltage deflections induced by periodic constant‐current hyperpolarizing pulses (0.2 nA, 0.2 Hz). D: top trace, spontaneous spikes prior to injection of LSD taken from point shown on average‐rate record (*). Bottom trace, last spontaneous firing of this cell before complete inhibition by LSD; taken from point shown on average‐rate record (**). Usual interspike depolarization does not occur after this spike.

From Aghajanian and VanderMaelen 7


Figure 4.

Frontal section through midbrain showing dorsal raphe neuron labeled with horseradish peroxidase. Enzyme was ejected into cell with depolarizing pulses (4 nA, 1 Hz, 900‐ms duration) applied for 4 min. Note polygonal or multipolar structure; somatic and dendritic spines were visible at higher magnifications. MLF, medial longitudinal fasciculus. Vibratone sections (100 μm) with cresyl violet acetate counterstain. Bars = 50 μm.

From Aghajanian and VanderMaelen 7


Figure 5.

Inhibitory responses of guinea pig hippocampal CA1 neurons to serotonin (5‐HT), recorded intracellularly. A: electrode positioned in CA1 region. ALV, alveus; OR, stratum oriens; PYR, stratum pyramidale; RAD, stratum radiatum; L‐M, stratum lacunosum‐moleculare; REC, recording electrode; 5‐HT, iontophoresis electrode; and STIM, stimulating electrode. B: membrane potential of neuron before (a), during (b), and after (c) iontophoresis with 5‐HT HCI (20 nA). Cell is hyperpolarized during 5‐HT iontophoresis. Membrane potential recordings are low‐pass filtered at 2 Hz during reproduction from tape recorder. C: cell input resistance before (a), during (b), and after (c) application of 5‐HT, measured with hyperpolarizing current pulses of 1 nA. Input resistance was decreased during 5‐HT application. D: same type of response as in C, but elicited with diffusion from glass pipette containing 10−3 M 5‐HT creatine sulfate. E: example of unbalanced (a) and balanced (b) recording electrode resistance.

From Jahnsen 77


Figure 6.

Effects of 5‐HT on inhibitory postsynaptic potential (IPSP). Intracellular recordings from rat hippocampus CA1 pyramidal neurons in vitro. A: specimen record of cellular membrane responses to 5‐HT applied by microdroplet at time indicated by arrow. Marked hyperpolarization associated with decrease in input resistance was recorded. Input resistance was measured by injecting constant‐current hyperpolarizing pulses. B: IPSP was produced by stimulation (arrow) near pyramidal layer. Inhibitory stimuli were applied simultaneously with series of hyperpolarizing current pulses (nA shown) to measure IPSP reversal potential (−68 mV). C: same as B, but after 5‐HT application. Membrane potential was slightly below IPSP reversal potential, and no IPSP was seen. An IPSP could still be produced by applying stimulation on top of depolarizing current pulse (+0.4 nA). D: current‐voltage plot of cell's responses to series of hyperpolarizing pulses, before and after 5‐HT application. Reversal potential for 5‐HT is ca. −83 mV. E: magnitude of IPSP at various potential levels before and after 5‐HT application (symbols as in D), indicating IPSP reversal potential that is not changed by 5‐HT.

From Segal 129


Figure 7.

Effect of extracellular K+ on membrane potential and resistance responses to 5‐HT applied by microdroplet (arrows). A: response to 5‐HT in normal (5 mM) K+ medium. B: same cell, after superfusion with 10 mM K+. Note change in potential (+10 mV) and smaller change in potential produced by 5‐HT. C: same cell, superfused with 10 mM K+ and hyperpolarized with continuous current. 5‐HT no longer produced hyperpolarization, although resistance change is evident.

From Segal 129


Figure 8.

Facilitation of glutamate‐induced excitation of rat facial motoneurons by 5‐HT. Singleunit activity was recorded extracellularly, and substances were applied by microiontophoresis. Ratemeter recordings in A, B, and C show number of spikes occurring in each 10‐s period. A: 5‐HT (10 nA) reduced threshold required for glutamate‐induced activation of unit. 5‐HT (200 nA) failed to directly excite neuron. B: facilitating effect of 1‐min pulses of 5‐HT on glutamate‐induced excitation (G, 2 nA) of motoneuron. C: facilitation of subthreshold excitatory effect of glutamate (G, 7 nA) by 5‐HT. D: cumulative dose‐response curve for glutamate‐induced excitation of rat facial motoneurons in presence (left) and absence (right) of 5‐HT (10 nA). Abscissa, duration of glutamate ejection. Ordinate, percentage of cells showing maximal excitation (overdepolarization) at given duration of glutamate ejection.

From McCall and Aghajanian 94


Figure 9.

Facilitation of glutamate‐evoked excitation of a rat spinal motoneuron by 5‐HT and norepinephrine (NA). Single‐unit activity was recorded extracellularly, and substances were applied by microiontophoresis. Height of bars indicates number of spikes fired during short application of glutamate, which was given repeatedly. Cells did not fire spontaneously in absence of glutamate. A: pre‐metergoline. 5‐HT and NA facilitation of glutamate‐evoked activity in this motoneuron was preceded by brief periods of inhibition during current application, specified in nA. B: post‐metergoline (1 mg/kg body wt, iv). Metergoline reduced glutamate‐evoked activity and prevented 5‐HT increase, but not NA increase, of evoked activity. C: recovery. Glutamate sensitivity recovered eventually, along with response to 5‐HT.

From White and Neuman 154


Figure 10.

Typical response of rat facial motoneuron (recorded intracellularly) to iontophoretically applied 5‐HT. Simultaneous pen recordings of resting membrane potential (A), neuronal input resistance (B), and number of spikes occurring during intracellularly injected depolarizing current pulse (C), which is measure of neuron excitability. A: resting membrane potential, with electrotonic displacements of membrane potential and spike potentials filtered out. B: amplitude of voltage displacements in response to 2.0‐nA hyperpolarizing pulses, with scale on right adjusted according to Ohm's law to give input resistance in MΩ. Bar between A and B indicates duration and ejection current of iontophoretically applied 5‐HT. C: output of spike counter, which was reset after each depolarizing pulse. All spikes were triggered by intracellular depolarizing current pulse, which occurred once every 2 s, and which was adjusted to 67% of threshold to fire 1 spike before 5‐HT was applied. D: oscilloscope traces (1–4) occurred at times indicated by arrows in A. Current monitor trace is shown at top. Time marker occurred once every 10 s, and applies to A‐C. Distance between iontophoretic and recording electrode tips was ∼45 μm. 5‐HT caused membrane depolarization, increased input resistance (Rinput) and excitability.

From VanderMaelen and Aghajanian, unpublished observations


Figure 11.

Responses of rat facial motoneuron to iontophoretically applied glycine (GLY), γ‐aminobutyric acid (GABA), and 5‐HT. A, B, and C: simultaneous pen recordings, as described in Fig. 10. Durations and amplitudes (in nA) of iontophoretic currents are indicated by bars below A. Membrane responses to GLY and GABA were depolarizing due to Cl− diffusion into cell from recording electrode, which contained 3 M KCI. Selected sweeps of oscilloscope are shown above A and occurred at times indicated by arrows. Current monitor trace is above each voltage‐recording trace. B: longer and shorter lines were caused by alternating 1.0‐ and 2.0‐nA hyperpolarizing current pulses, 1 pulse/s. Scale to right in B is for larger (2.0 nA) pulses only. No depolarizing current pulses were injected. Spike activity was spontaneous (i.e., not evoked by depolarizing current pulses). This experiment indicates that 5‐HT response is not due to decrease in membrane conductance of Cl−.

From VanderMaelen and Aghajanian 143


Figure 12.

Effects of depolarizing and hyperpolarizing current injections on membrane potential responses of rat facial motoneuron to iontophoretically applied 5‐HT and excitatory amino acid DL‐homocysteic acid (DLH). In each case DLH was ejected at 40 nA for 20 s, and 5‐HT was ejected at 154 nA for 50 s. Cell membrane was continuously depolarized or hyperpolarized by injection of current; amplitude of current is shown (in nA) to right of each trace. C: control responses when no current was injected into neuron. Resting potential in control condition was −72 mV and antidromic spike amplitude (not shown) was 92 mV. Time and voltage calibrations in A also apply to B‐E. Hyperpolarizing neuron by current injection abolished response to 5‐HT but had little effect on response to DLH.

From VanderMaelen and Aghajanian 143
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Article Title: Specific Systems of the Reticular Core: Serotonin
 

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G. K. Aghajanian, C. P. Vandermaelen. Specific Systems of the Reticular Core: Serotonin. Compr Physiol 2011, Supplement 4: Handbook of Physiology, The Nervous System, Intrinsic Regulatory Systems of the Brain: 237-256. First published in print 1986. doi: 10.1002/cphy.cp010404