From stimulation to undulation: a neuronal pathway for the control of swimming in the leech.

Initiation and performance of the swimming movement in the leech (Hirudo medicinalis) are controlled by neurons organized at at least four functional levels-sensory neurons, gating neurons, oscillator neurons, and motor neurons. A paired neuron, designated as Trl, in the subesophageal ganglion of the leech has now been shown to define a fifth level, interposed between sensory and gating neurons. Cell Trl is activated by pressure and nociceptive mechanosensory neurons, which mediate bodywall stimulus-evoked swimming activity in intact leeches. In the isolated leech nervous system, brief stimulation of cell Trl elicits sustained activation of the gating neurons and triggers the onset of swimmning activity. The synaptic interactions between all five levels of control are direct. Discovery of the Trl cells thus completes the identification of a synaptic pathway by which mechanosensory stimulation leads to the swimming movements of the leech.

Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes.

We show that neurons that underlie rhythmic patterns of electrical output may be identified by optical imaging and frequency-domain analysis. Our contrast agent is a two-component dye system in which changes in membrane potential modulate the relative emission between a pair of fluorophores. We demonstrate our methods with the circuit responsible for fictive swimming in the isolated leech nerve cord. The output of a motor neuron provides a reference signal for the phase-sensitive detection of changes in fluorescence from individual neurons in a ganglion. We identify known and possibly novel neurons that participate in the swim rhythm and determine their phases within a cycle. A variant of this approach is used to identify the postsynaptic followers of intracellularly stimulated neurons.

Identified neurons and leech swimming behavior.

Since the experiments of Nicholls and Baylor, the initial characterization of identified neurons has provided significant insight into the circuitry transforming mechanosensory input into the motor output of swimming. From physiological characterization of only a small percentage of cells within the leech CNS, we have gained important information about how the decision to swim is processed and how the rhythmic motor pattern is generated. While many of the synaptic connections in the swim-generating circuit have been identified, the elucidation of the biophysical and biochemical mechanisms underlying these connections has only recently begun. The observation that constant input can result in variable motor output suggests that, in addition to describing a cell's identity in terms of structure and function, factors such as behavioral context and the "internal state" of the nervous system must also be considered. As circuits controlling other behaviors become known, one can examine the interactions between these networks to understand issues of behavioral choice at the level of identified neurons. The leech CNS has expanded our understanding of how the nervous system produces behavior and continues to serve as an excellent model in this endeavor.

Glutamate receptor 5/6/7-like and glutamate transporter-1-like immunoreactivity in the leech central nervous system.

Previous physiological and pharmacological evidence has suggested a neurotransmitter role for the excitatory amino acid glutamate in the leech central nervous system (CNS). In the present study, we sought to localize glutamate receptor (GluR) subunits (GluR 5/6/7, GluR 2/3 and N-methyl-D-aspartate receptor 1 [NMDAR 1]) and a glutamate transporter subtype [GLT-1] within the leech CNS using mono- and polyclonal antibodies. In whole-mounted tissue, small cells of the outer capsule and putative microglia labeled with both GluR 5/6/7 and GluR 2/3 but not NMDAR 1 subunit antisera. In general, GluR 5/6/7-like immunofluorescence was both more intense and more widespread than GluR 2/3-like immunolabeling. Cryostat-sectioned tissue revealed extensive GluR 5/6/7-like immunoreactivity throughout the neuropil as well as labeling within a few neuronal somata. GLT-1-like immunoreactivity localized to the inner capsule, which is the interface between neuronal somata and the neuropil and is deeply invested by processes of neuropil glia. These results complement previous physiological and pharmacological findings indicating that the leech CNS possesses the cellular machinery to respond to glutamate and to transport glutamate from extracellular spaces. Together, they provide further evidence for glutamate's role as a neurotransmitter within the leech CNS.

The role of glutamate in swim initiation in the medicinal leech.

Antagonists were used to investigate the role of the excitatory amino acid, L-glutamate, in the swim motor program of Hirudo medicinalis. In previous experiments, focal application of L-glutamate or its non-NMDA agonists onto either the segmental swim-gating interneuron (cell 204) or the serotonergic Retzius cell resulted in prolonged excitation of the two cells and often in fictive swimming. Since brief stimulation of the subesophageal trigger interneuron (cell Tr1) evoked a similar response, we investigated the role of glutamate at these synapses. Kynurenic acid and two non-NMDA antagonists, 6,7-dinitroquinoxaline-2,3-dione (DNQX) and Joro spider toxin, effectively suppressed (1) the sustained activation of cell 204 and the Retzius cell following cell Tr1 stimulation and (2) the monosynaptic connection from cell Tr1 to cell 204 and the Retzius cell, but did not block spontaneous or DP nerve-activated swimming. Other glutamate blockers, including gamma-D-glutamylaminomethyl sulfonic acid, L(+)-2-amino-3-phosphonoproprionic acid and 2-amino-5-phosphonopentanoic acid, were ineffective. DNQX also blocked both indirect excitation of cell 204 and direct depolarization of cell Tr1 in response to mechanosensory P cell stimulation. Our findings show the involvement of non-NMDA receptors in activating the swim motor program at two levels: (1) P cell input to cell Tr1 and (2) cell Tr1 input to cell 204, and reveal an essential role for glutamate in swim initiation via the cell Tr1 pathway.

Effect of auditory deafferentation on the synaptic connectivity of a pair of identified interneurons in adult field crickets.

In adult crickets, Teleogryllus oceanicus, unilateral auditory deafferentation causes the medial dendrites of an afferent-deprived, identified auditory interneuron (Int-1) in the prothoracic ganglion to sprout and form new functional connections in the contralateral auditory neuropil. The establishment of these new functional connections by the deafferented Int-1, however, does not appear to affect the physiological responses of Int-1's homolog on the intact side of the prothoracic ganglion which also innervates this auditory neuropil. Thus it appears that the sprouting dendrites of the deafferented Int-1 are not functionally competing with those of the intact Int-1 for synaptic connections in the remaining auditory neuropil following unilateral deafferentation in adult crickets. Moreover, we demonstrate that auditory function is restored to the afferent-deprived Int-1 within 4-6 days following deafferentation, when few branches of Int-1's medial dendrites can be seen to have sprouted. The strength of the physiological responses and extent of dendritic sprouting in the deafferented Int-1 progressively increase with time following deafferentation. By 28 days following deafferentation, most of the normal physiological responses of Int-1 to auditory stimuli have been restored in the deafferented Int-1, and the medial dendrites of the deafferented Int-1 have clearly sprouted and grown across into the contralateral auditory afferent field. The strength of the physiological responses of the deafferented Int-1 to auditory stimuli and extent of dendritic sprouting in the deafferented Int-1 are greater in crickets deafferented as juveniles than as adults. Thus, neuronal plasticity persists in Int-1 following sensory deprivation from the earliest juvenile stages through adulthood.

Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion. II. Role of segmental swim-initiating interneurons.

Cell Tr1, a trigger neuron found in the subesophageal ganglion of the leech, Hirudo medicinalis, is part of a network of subesophageal ganglion neurons which control swimming activity, and makes apparently direct connections to swim-initiating interneurons (SIIs; cells 204 and 205). In this study, we investigated the role of SIIs in swim initiation by cell Tr1. We also examined how brief Tr1 activity controls swim initiation at the levels of the SIIs and of the oscillator neurons. We found: In shortened nerve cord preparations consisting of the head ganglion (supra- and subesophageal ganglia) through segmental ganglia 11 or 12, the effectiveness of swim initiation by Tr1 stimulation was highly correlated with the concurrent injection of depolarizing or hyperpolarizing current into a single cell 204. Tr1 stimulation causes sustained excitation in SIIs, serotonin-containing interneurons and Retzius cells, independent of whether or not swimming is initiated. A short, depolarizing current pulse injected simultaneously into as many as three 204 cells does not replicate the sustained excitation evoked in these cells by Tr1 stimulation. An oscillator neuron, cell 208, is inhibited when Tr1 stimulation fails to elicit swimming, but receives excitatory input from Tr1 otherwise. In another oscillator neuron, cell 115, stimulation of Tr1 suppressed an unidentified source of inhibitory synaptic potentials only on trials which resulted in swim initiation. We conclude that Tr1 stimulation triggers swimming by activating a long-lasting ramp depolarization in the SIIs which, in turn, provide excitatory drive to the swim oscillator. Moreover, Tr1 initiates swimming only when inhibitory inputs to the swim oscillator are suppressed.(ABSTRACT TRUNCATED AT 250 WORDS)

Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion. III. Sensory inputs to Tr1 and Tr2.

In papers I and II of this series, we described two pairs of interneurons, Tr1 and Tr2, in the leech subesophageal ganglion which can trigger swimming activity in the isolated central nervous system (CNS). In this paper, we describe sensory inputs to these trigger neurons from previously identified mechanosensory neurons. We found that: Weak mechanical stimulation (stroking) of a body wall flap attached to a segmental ganglion in an otherwise isolated CNS excites the contralateral Tr1 slightly. Strong mechanical stimulation (pinching) of a mid-body wall flap evokes a burst of impulses in the contralateral Tr1. For both means of stimulation the effects on the ipsilateral Tr1 and on the Tr2 cell pair were much weaker. Stroking a body wall flap attached to the head ganglion (supra- and subesophageal ganglia) in an otherwise isolated CNS excites both Tr1s and both Tr2s, although the effect is weaker for the Tr2s. Pinching strongly excites both trigger neurons bilaterally. Pressure and nociceptive mechanosensory neurons (P and N cells) in the subesophageal ganglion and the first segmental ganglion appear to make direct excitatory synapses with the contralateral Tr1 and Tr2. Mechanosensory interactions with the ipsilateral trigger neurons appear to be indirect. Functional inactivation of Tr1 by hyperpolarization does not prevent swim initiation either by weak mechanical stimulation of a body-wall flap or by intracellular stimulation of P cells.2+ We conclude that the trigger neurons, Tr1 and Tr2, provide an excitatory pathway by which mechanosensory stimulation can initiate leech swimming activity.(ABSTRACT TRUNCATED AT 250 WORDS)

Ultrasound sensitive neurons in the cricket brain.

1. The aim of this study was to identify neurons in the brain of the cricket, Teleogryllus oceanicus, that are tuned to high frequencies and to determine if these neurons are involved in the pathway controlling negative phonotaxis. In this paper we describe, both morphologically and physiologically, 20 neurons in the cricket brain which are preferentially tuned to high frequencies. 2. These neurons can be divided into two morphological classes: descending brain interneurons (DBINs) which have a posteriorly projecting axon in the circumesophageal connective and local brain neurons (LBNs) whose processes reside entirely within the brain. All the DBINs and LBNs have processes which project into one common area of the brain, the ventral brain region at the border of the protocerebrum and deutocerebrum. Some of the terminal arborizations of Int-1, an ascending ultrasound sensitive interneuron which initiates negative phonotaxis, also extend into this region. 3. Physiologically, ultrasonic sound pulses produce 3 types of responses in the DBINs and LBNs. (1) Seven DBINs and 6 LBNs are excited by ultrasound. (2) Ongoing activity in one DBIN and 5 LBNs is inhibited by ultrasound, and (3) one cell, (LBN-ei), is either excited or inhibited by ultrasound depending on the direction of the stimulus. 4. Many of the response properties of both the DBINs and LBNs to auditory stimuli are similar to those of Int-1. Specifically, the strength of the response, either excitation or inhibition, to 20 kHz sound pulses increases with increasing stimulus intensity, while the response latency generally decreases. Moreover, the thresholds to high frequencies are much lower than to low frequencies. These observations suggest that the DBINs and LBNs receive a majority of their auditory input from Int-1. However, the response latencies and directional sensitivity of only LBN-ei suggest that it is directly connected to Int-1. 5. The response of only one identified brain neuron, DBIN8, which is inhibited by 20 kHz sound pulses, is facilitated during flight compared to its response at rest. This suggests that suppression of activity in DBIN8 may be associated with ultrasound-induced negative phonotactic steering responses in flying crickets. The other DBINs and LBNs identified in this paper may also play a role in negative phonotaxis, and possibly in other cricket auditory behaviors influenced by ultrasonic frequencies.

Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion. I. Output connections of Tr1 and Tr2.

The aim of this study was to identify neurons in the subesophageal ganglion of the medicinal leech which initiate swimming activity and to determine their output connections. We found two bilaterally symmetrical pairs of interneurons, Tr1 and Tr2, located in the first division of the subesophageal ganglion which initiate swimming activity in the isolated nervous system when depolarized with brief (1-3 s) current pulses. Tr1 and Tr2 are considered trigger neurons because elicited swimming episodes outlast the stimulus duration, and because the length of elicited swim episodes is nearly independent of the intensity with which Tr1 and Tr2 are stimulated. Tr1 and Tr2 have similar morphologies. The neurites of both cells cross contralaterally in the subesophageal ganglion, project posteriorly, and exit the subesophageal ganglion in the contralateral connective. The axons of Tr1 and Tr2 extend as far posterior as segmental ganglion 18 of the ventral nerve cord. Tr1 provides direct excitatory drive to three groups of segmental neurons which are capable of initiating swimming: swim-initiating interneurons (cells 204 and 205), serotonin-containing interneurons (cells 61 and 21), and the serotonergic Retzius cells. In addition, all Retzius cells in the subesophageal ganglion are excited directly by Tr1. These three groups of neurons are excited even if Tr1 stimulation is subthreshold for swim initiation. In contrast to Tr1, Tr2 stimulation evokes transient inhibition in swim-initiating and serotonin-containing interneurons, and has little immediate effect on Retzius cells. In addition, Tr2 indirectly inhibits several oscillator neurons, including cells 208, 33, and 60. When Tr1 is stimulated during a swimming episode the swim period decreases for several cycles, while stimulation of Tr2 during swimming episodes reliably resets the ongoing swimming rhythm. Our findings indicate that Tr1 and Tr2 are trigger neurons which initiate swimming activity by different pathways. These neurons also have functional interactions with the swim oscillator network since either Tr1 or Tr2 stimulation during swimming can modulate the ongoing swimming rhythm.

Control of leech swimming activity by the cephalic ganglia.

We investigated the role played by the cephalic nervous system in the control of swimming activity in the leech, Hirudo medicinalis, by comparing swimming activity in isolated leech nerve cords that included the head ganglia (supra- and subesophageal ganglia) with swimming activity in nerve cords from which these ganglia were removed. We found that the presence of these cephalic ganglia had an inhibitory influence on the reliability with which stimulation of peripheral (DP) nerves and intracellular stimulation of swim-initiating neurons initiated and maintained swimming activity. In addition, swimming activity recorded from both oscillator and motor neurons in preparations that included head ganglia frequently exhibited irregular bursting patterns consisting of missed, weak, or sustained bursts. Removal of the two head ganglia as well as the first segmental ganglion eliminated this irregular activity pattern. We also identified a pair of rhythmically active interneurons, SRN1, in the subesophageal ganglion that, when depolarized, could reset the swimming rhythm. Thus the cephalic ganglia and first segmental ganglion of the leech nerve cord are capable of exerting a tonic inhibitory influence as well as a modulatory effect on swimming activity in the segmental nerve cord.

Integration of ultrasound and flight inputs on descending neurons in the cricket brain.

In response to ultrasonic stimuli, tethered flying crickets perform evasive steering movements that are directed away from the sound source (negative phonotaxis). In this study we have investigated the responsiveness to ultrasound of neurons that descend from the cricket brain, and whether flight activity facilitates the responsiveness of these neurons. 1. Ultrasonic stimuli evoke descending activity in the cervical connectives both ipsilateral and contralateral to the sound source. 2. Both the amount of descending activity and the latency of this response in the cervical connectives are linearly correlated with ultrasonic stimulus intensity, regardless of the cricket's behavioral state. 3. Flight activity significantly increases the amount of descending activity evoked by ultrasound at all stimulus intensities, and significantly decreases the latency of the response in the cervical connectives compared with non-flying crickets. Flight activity, however, does not significantly affect the activity in an interneuron (Int-1) carrying ultrasound input to the brain. Thus, the increase in the amount of descending activity produced during flight activity is due to the integration of input from Int-1 and the flight motor system to ultrasound-sensitive neurons in the cricket brain. 4. Descending units recorded in the cervical connectives originate in the cricket brain. A reduction in the amount of descending activity is correlated with a decrease in the magnitude of the negative phonotactic response of the abdomen during flight activity, suggesting that these descending units play a role in eliciting negative phonotaxis.

Glutamate-like immunoreactivity in the leech central nervous system.

Using a monoclonal antibody for glutamate the distribution was determined of glutamate-like immunoreactive neurons in the leech central nervous system (CNS). Glutamate-like immunoreactive neurons (GINs) were found to be localized to the anterior portion of the leech CNS: in the first segmental ganglion and in the subesophageal ganglion. Exactly five pairs of GINs consistently reacted with the glutamate antibody. Two medial pairs of GINs were located in the subesophageal ganglion and shared several morphological characteristics with two medial pairs of GINs in the first segmental ganglion. An additional lateral pair of GINs was also located in segmental ganglion 1. A pair of glutamate-like immunoreactive neurons, which are potential homologs of the lateral pair of GINs in segmental ganglion 1, were occasionally observed in more posterior segmental ganglia along with a selective group of neuronal processes. Thus only a small, localized population of neurons in the leech CNS appears to use glutamate as their neurotransmitter.

Neuronal factors influencing the decision to swim in the medicinal leech.

The initiation of leech (Hirudo medicinalis) swimming in isolated segmental nerve cord preparations requires only excitation of segmental swim gating and swim oscillatory interneurons. However, several observations indicate that when the entire isolated central nervous system (head ganglion through tail ganglion) is used, neuronal inputs from the head ganglion other than excitatory inputs to the segmental swim-generating network influence whether swimming results in response to a given stimulus. In this study, experiments were performed to demonstrate that the initiation of swimming is controlled by two parallel pathways emanating from the head ganglion that have opposite effects on the segmental swim-generating network. One pathway, the swim-activating system, excites the segmental swim-generating network, while the other pathway, the swim-inactivating system, suppresses it. The balance between the effects that the swim-activating and inactivating systems have on the segmental swim-generating network determines whether swimming occurs. Moreover, we identified a pair of interneurons, cells SIN1, in the leech head ganglion whose spiking activity must be suppressed in order for swimming to be initiated since their activity is incompatible with swimming. Depolarization of cell SIN1 during swimming indirectly inhibits segmental swim-gating interneurons and terminates ongoing swimming activity. Thus, cells SIN1 are most likely part of the swim-inactivating system in the leech head ganglion.

A sensory system initiating swimming activity in the medicinal leech.

1. Water-wave stimulation, which was previously shown to elicit swimming in intact leeches, can initiate swimming in a semi-intact leech preparation via activation of the sensillar movement receptors (SMRs), provided that 50 micron-serotonin is added to the physiological saline. 2. The neuronal responses resulting from near-field stimulation of the leech body wall with a vibrating probe were recorded in peripheral nerves and in nerve-cord connectives. The response in the dorsal posterior nerve to a single vibratory pulse consists of a graded compound action potential.The units contributing to this action potential have a much lower threshold for near-field stimulation than do touch cells. They appear to be the same sensory units, the SMRs, that mediate leech sensitivity to water waves. 3. The frequency domain of the SMR sensitivity extends as low as 1 Hz. Thus, leeches could receive self-stimulation from the water vibrations created by their own swimming movements. 4. Leech physiological saline containing 20-40 m-Mg² does not eliminate the SMR response to near-field stimulation recorded in the DP nerve;however, elevated Mg² concentrations do eliminate the neuronal responses in the nerve cord connectives. Thus, while no chemical synapse occurs between the peripherally situated SMRs and nerve cord ganglia, a synapse may be interposed between the SMRs and the intersegmental neurones activated by near-field stimulation.5. The swim-facilitating action of serotonin occurs at unidentified sites within the ventral nerve cord, since serotonin does not alter the sensitivity of the SMRs.

Kinematic and aerodynamic aspects of ultrasound-induced negative phonotaxis inflying Australian field crickets (Teleogryllus oceanicus).

Negative phonotaxis is elicited in flying Australian field crickets, Teleogryllus oceanicus, by ultrasonic stimuli. Using upright tethered flying crickets, we quantitatively examined several kinematic and aerodynamic factors which accompany ultrasound-induced negative phonotactic behavior. These factors included three kinematic effects (hindwing wingbeat frequency, hindwing elevation and depression, and forewing tilt) and two aerodynamic effects (pitch and roll). 1. Within two cycles following a 20 dB suprathreshold ultrasonic stimulus, the hindwing wingbeat frequency increases by 3-4 Hz and outlasts the duration of the stimulus. Moreover, the relationship between the maximum increase in wingbeat frequency and stimulus intensity is a two-stage response. At lower suprathreshold intensities the maximum wingbeat frequency increases by approximately 1 Hz; but, at higher intensities, the maximum increase is 3-4 Hz. 2. The maximum hindwing elevation angle increases on the side ipsilateral to the stimulus, while there was no change in upstroke elevation on the side contralateral to the stimulus. 3. An ultrasonic stimulus affects forewing tilt such that the forewings bank into the turn. The forewing ipsilateral to the stimulus tilts upward while the contralateral forewing tilts downward. Both the ipsilateral and contralateral forewing tilt change linearly with stimulus intensity. 4. Flying crickets pitch downward when presented with a laterally located ultrasonic stimulus. Amputation experiments indicate that both the fore and hindwings contribute to changes in pitch but the pitch response in an intact cricket exceeds the simple addition of fore and hindwing contributions. With the speaker placed above or below the flying cricket, the change is downward or upward, respectively.(ABSTRACT TRUNCATED AT 250 WORDS)

Regulation of the segmental swim-generating system by a pair of identified interneurons in the leech head ganglion.

1. The aim of this study was to identify neurons that modulate activity of segmental swim gating interneurons. We found a pair of bilaterally symmetrical interneurons, cells SE1, whose activity level directly influences three groups of segmental neurons associated with generating swimming in the medicinal leech. 2. The somata of cells SE1 are located on the dorsal surface of the subesophageal ganglion. Their axons extend most, if not the entire, length of the ventral nerve cord and appear to make identical connections with the same group of swim-generating neurons in all segmental ganglia. 3. Cells SE1 excite monosynaptically all segmental swim gating interneurons, cells 204, examined. The level of excitation in cell 204 is directly correlated with the firing frequency of cell SE1. In most quiescent preparations (when the preparation is not swimming) hyperpolarization of a single cell SE1 eliminates all excitatory synaptic input to cells 204. 4. Cells SE1 excite monosynaptically three swim oscillatory interneurons, cells 115, 28, and 208. The strength of the connection from cell SE1 to cell 115 is stronger than the connection from cell SE1 to either cells 28 or 208. The level of excitation in cell 115 is directly correlated with the firing frequency of cell SE1. In most quiescent preparations, hyperpolarization of a single cell SE1 eliminates all excitatory synaptic input to cell 115 but has only a minor effect on the level of activity in cells 208 and 28. 5. Due most likely to the strong and direct connections cells SE1 have with swim gating and oscillatory interneurons, brief stimulation of cell SE1 can elicit swimming. Swimming generally occurs within 1 s after stimulation of cell SE1. During swimming, the membrane potential of cell SE1 depolarizes by 2-5 mV, and its firing frequency increases. Brief depolarization of cell SE1 during swimming reliably shifts the phase of the swimming rhythm, whereas longer periods of depolarization increase both swim period and burst duration. 6. Excitatory motor neurons to the dorsal longitudinal muscles, cells 3, 5, and 7, are strongly excited by stimulation of cell SE1. The firing frequency of cell 3 is positively correlated with the firing frequency of cell SE1. 7. The results of this study indicate that cells SE1 can modulate the level of excitation in three groups of neurons associated with generating leech swimming.(ABSTRACT TRUNCATED AT 400 WORDS)

Neuronal control of leech swimming.

Leech swimming is produced by the antiphasic contractions of dorsal and ventral longitudinal muscles that travel rearward along the animal and propel it forward. Research over the past three decades has focused on identifying the underlying neuronal circuit and mechanisms that produce and control this coordinated movement pattern. Investigations have also tested whether leech swimming is modifiable, both by experience and by neuromodulators. One outcome has been the identification of several functional classes of neurons associated with swimming. Systematic analysis of the interactions between these neurons had led to the elucidation of a neuronal circuit that adequately accounts for the generation of the swim motor program cord. The swim motor program appears to be produced by a chain of coupled segmental oscillators whose intrinsic properties and intersegmental connections ensure the coordinated expression of swimming along the nerve cord. In addition, neurons identified in the head ganglion comprise two parallel, but opposite-acting, systems that control the initiation of swimming in response to sensory input. Also, the pathway by which body wall stimulation initiates swimming shows a simple form of learning, that is habituation. Repeatedly stroking the leech body wall decreases both the probability of initiating swimming and the length of elicited swim episodes. Finally, the biogenic amine serotonin, which is found in the nerve cord, affects leech swimming in a number of ways. Serotonin's modulation of swimming is due, in part, to its effect of the membrane properties of swim-initiating interneurons and several swim motor neurons.

Effect of the tail ganglion on swimming activity in the leech.

In the medicinal leech, Hirudo medicinalis, isolated segmental nerve cords are capable of generating swimming activity. The role played by the head and tail ganglia in regulating the expression of swimming activity by the segmental nerve cord was evaluated by comparing swimming activity in nerve cord preparations with and without the head and tail ganglia attached. Several swim properties were examined, including length of induced swim episodes, ability to initiate swim episodes, swim cycle period, and phase. We found that, in general, the presence of the tail ganglion attached to isolated nerve cords countered the effects produced by the head ganglion on swimming activity. Moreover, we observed that the tail ganglion itself provides excitatory drive to the swim generating system. Thus, the inputs from the head and tail ganglia influence significantly the expression of swimming activity.