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PubMed2004

Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons.

The performance of the brain is constrained by wiring length and maintenance costs. The apparently inverse relationship between number of neurons in the various interneuron classes and the spatial extent of their axon trees suggests a mathematically definable organization, reminiscent of 'small-world' or scale-free networks observed in other complex systems. The wiring-economy-based classification of cortical inhibitory interneurons is supported by the distinct physiological patterns of class members in the intact brain. The complex wiring of diverse interneuron classes could represent an economic solution for supporting global synchrony and oscillations at multiple timescales with minimum axon length.

Animals↗
PubMed2003

Interneuron Diversity series: Interneuron research--challenges and strategies.

The field of interneuron research has come of age. An influx of new data has shed light on many areas, but has also highlighted major challenges. The articles in this review series will address several of these challenges, including developing a standardized classification scheme, defining how the integrative properties of interneurons shape their functional roles (including the generation of oscillatory activity), and identifying molecular mechanisms of synaptic plasticity. New technologies can help us address these problems in ways not previously possible. To coordinate the vast amount of data being generated, we propose the creation of a world-wide-web Interneuron Database that will facilitate inter-laboratory comparisons and collaborative studies. A well-crafted database has the potential to bring new insight by standardizing and organizing data collected in physiological, anatomical and molecular studies.

Animals↗
PubMed2002

Innervation of interneurons immunoreactive for VIP by intrinsically bursting pyramidal cells and fast-spiking interneurons in infragranular layers of juvenile rat neocortex.

Cortical columns contain specific neuronal populations with characteristic sets of connections. This wiring forms the structural basis of dynamic information processing. However, at the single-cell level little is known about specific connectivity patterns. We performed experiments in infragranular layers (V and VI) of rat somatosensory cortex, to clarify further the input patterns of inhibitory interneurons immunoreactive (ir) for vasoactive intestinal polypeptide (VIP). Neurons in acute slices were electrophysiologically characterized using whole-cell recordings and filled with biocytin. This allowed us to determine their firing pattern as regular-spiking, intrinsically bursting and fast-spiking, respectively. Biocytin was revealed histochemically and VIP immunohistochemically. Sections were examined for contacts between the axons of the filled neurons and the VIP-ir targets. Twenty pyramidal cells and five nonpyramidal (inter)neurons were recovered and sufficiently stained for further analysis. Regular-spiking pyramidal cells displayed no axonal boutons in contact with VIP-ir targets. In contrast, intrinsically bursting layer V pyramidal cells showed four putative single contacts with a proximal dendrite of VIP neurons. Fast-spiking interneurons formed contacts with two to six VIP neurons, preferentially at their somata. Single as well as multiple contacts on individual target cells were found. Electron microscopic examinations showed that light-microscopically determined contacts represent sites of synaptic interactions. Our results suggest that, within infragranular local cortical circuits, (i) fast-spiking interneurons are more likely to influence VIP cells than are pyramidal cells and (ii) pyramidal cell input probably needs to be highly convergent to fire VIP target cells.

Action Potentials↗
PubMed1995

Intrinsic neuromodulation in the Tritonia swim CPG: the serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2.

Heterosynaptic enhancement of transmitter release is potentially very important for neuronal computation, yet, to our knowledge, no prior study has shown that stimulation of one neuron directly enhances release from an interneuron. Here, we demonstrate that in the marine mollusk Tritonia diomedea, the serotonergic dorsal swim interneurons (DSIs) heterosynaptically increase the amount of transmitter released from another interneuron, C2. Stimulation of a single DSI at physiological firing frequencies increases the size of synaptic potentials evoked by C2. This increase in synaptic efficacy is correlated with an increase in homosynaptic paired-pulse facilitation by C2. Thus, it is likely to be due to an enhancement of transmitter release from C2, rather than a postsynaptic action on the followers of C2. This is further supported by the fact that DSI stimulation enhances the strengths of all chemical synapses made by C2 within the swim network, regardless of their sign. Furthermore, DSI enhances the amplitude of C2 synaptic potentials recorded in neurons that DSI itself does not synapse with. Finally, DSI differentially modulates different synaptic inputs to the same postsynaptic target; while increasing C2-evoked EPSPs it simultaneously decreases the size of EPSPs evoked by other DSIs. The heterosynaptic facilitation of C2 synaptic potentials by DSI is not caused by a simple depolarization of C2, but may be a direct action on the transmitter release mechanism. This neuromodulatory effect, which is intrinsic to the circuitry of the central pattern generator for escape swimming in Tritonia, may be important for self-reconfiguration of the swim motor network.

Animals↗
PubMed1996

Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus.

Spine-free calretinin-immunoreactive (CR-IR) interneurons form a subpopulation of GABAergic cells in the rat hippocampus. A characteristic feature of these cells--located in all areas and layers--is the frequent dendro-dendritic and axo-dendritic contacts they form with each other. In this study we examined in detail the connectivity of these neurons by reconstructing their dendritic and axonal arbor and by identifying their postsynaptic targets. Radially running dendrites of CR-IR cells, located in different layers, intermingled into long braids. An average cell was in contact with dendrites of three to seven other CR-IR cells. Reconstruction of the dendritic trees from six consecutive sections demonstrated that at least 15 cells may participate in a dendro-dendritically connected cluster. Electron microscopical examination revealed that regularly spaced zonula adherentia connect the touching dendrites. The postsynaptic targets of CR-IR neurons have been examined using postembedding immunogold staining for GABA. CR-containing GABA-immunoreactive axons of local origin formed multiple symmetrical synaptic contacts (two to five) exclusively on GABAergic dendrites (CR-negative as well as CR-positive). Two to 10 CR-IR axons may converge onto a single CR-IR neuron, often from cells belonging to the same dendro-dendritically connected cluster. Using double immunocytochemistry, CR-IR cells were shown to heavily innervate calbindin D28k-containing interneurons and VIP-containing basket cells but avoided the parvalbumin-containing basket and axo-axonic cells. The unique connectivity of CR-IR cells may enable them to play a crucial role in the generation of synchronous, rhythmic hippocampal activity by controlling other interneurons terminating on different dendritic and somatic compartments of principal cells.

Animals↗
PubMed1984

The large fourth abdominal intersegmental interneuron: a new type of wind-sensitive ventral cord interneuron in locusts.

A large interneuron in Locusta migratoria is described that extends from the fourth abdominal ganglion to the brain. The morphology was revealed by injection of cobaltous ions or Lucifer yellow into the cell. As its cell body lies within the fourth abdominal ganglion it is named A4I1, the first-identified intersegmental interneuron of the fourth abdominal ganglion. This neuron receives input from highly flexible, wind-sensitive hairs on the prosternum, the pronotum, and the head (field 1). Sensory connections with A4I1 are made within the prothoracic ganglion. Stimulation of the receptive field initiates spikes in A4I1 which travel anteriorly and posteriorly from the prothoracic ganglion. Intracellular recording from the axon and the soma shows that the cell membrane becomes inactive within the fourth abdominal ganglion. Spikes could be generated within the fourth abdominal ganglion by current injection into the soma. Occasionally excitatory postsynaptic potentials were observed in a soma recording, but up to now there is no evidence for a second spike initiation site. By intracellular current injection into the soma of the left and right A4I1 cell it is shown that the two cells are not electrically coupled.

Afferent Pathways↗
PubMed1992

Evidence that synaptic transmission between giant interneurons and identified thoracic interneurons in the cockroach is cholinergic.

In the cockroach, a population of thoracic interneurons (TIs) receives direct inputs from a population of ventral giant interneurons (vGIs). Synaptic potentials in type-A TIs (TIAs) follow vGI action potentials with constant, short latencies at frequencies up to 200 Hz. These connections are important in the integration of directional wind information involved in determining an oriented escape response. The physiological and biochemical properties of these connections that underlie this decision-making process were examined. Injection of hyperpolarizing or depolarizing current into the postsynaptic TIAs resulted in alterations in the amplitude of the post-synaptic potential (PSP) appropriate for a chemical connection. In addition, bathing cells in zero-calcium, high-magnesium saline resulted in a gradual decrement of the PSP, and ultimately blocked synaptic transmission, reversibly. Single-cell choline acetyltransferase (ChAT) assays of vGI somata were performed. These assays indicated that the vGIs can synthesize acetylcholine. Furthermore, the pharmacological specificity of transmission at the vGI to TIA connections was similar to that previously reported for nicotinic, cholinergic synapses in insects, suggesting that the transmitter released by vGIs at these synapses is acetylcholine.

Acetylcholine↗
PubMed1992

Biogenic amines modulate synaptic transmission between identified giant interneurons and thoracic interneurons in the escape system of the cockroach.

In the escape system of the cockroach, Periplaneta americana, a population of uniquely identifiable thoracic interneurons (type A or TIAs) receive information about wind via chemical synapses from a population of ventral giant interneurons (vGIs). The TIAs are involved in the integration of sensory information necessary for orienting the animal during escape. It is likely that there are times in an animal's life when it is advantageous to modify the effectiveness of synaptic transmission between the vGIs and the TIAs. Given the central position of the TIAs in the escape system, this would greatly alter associated motor outputs. We tested the ability of octopamine, serotonin, and dopamine to modulate synaptic transmission between vGIs and TIAs. Both octopamine and dopamine significantly increased the amplitude of vGI-evoked excitatory postsynaptic potentials (EPSPs) in TIAs at 10(-4)-10(-2) M, and 10(-3) M, respectively. On the other hand, serotonin significantly decreased the vGI-evoked EPSPs in TIAs at 10(-4)-10(-3) M. These results indicate that octopamine, serotonin, and dopamine are capable of modulating the efficacy of transmission of important neural connections within this circuit.

Animals↗
PubMed2003

Interneuron Diversity series: Hippocampal interneuron classifications--making things as simple as possible, not simpler.

The nervous system is made up of many specific types of neuron intricately intertwined to form complex networks. Identifying and defining the characteristic features of the many different neuronal types is essential for achieving a cellular understanding of complex activity from perception to cognition. So far, cortical GABAergic interneurons have represented the epitome of cellular diversity in the CNS. Despite the desperate need for effective classification criteria allowing a common language among neuroscientists, interneurons still evoke memories of Babel. Several approaches are now available to overcome the challenges and problems associated with the various classification systems used so far.

Animals↗
PubMed2003

Interneuron diversity series: inhibitory interneurons and network oscillations in vitro.

In vitro models of rhythms of cognitive relevance, such as gamma (30-80 Hz) and theta (5-12 Hz) rhythms in the hippocampus, demonstrate an absolute requirement for phasic inhibitory synaptic transmission. Such rhythms can occur transiently, of approximately 1 s duration, or persistently, lasting for many hours. In the latter case, stable patterns of interneuron output, and their postsynaptic consequences for pyramidal cell membrane potential, occur despite known constraints of synaptic habituation and potentiation. This review concentrates on recent in vitro evidence revealing a division of labour among different subclasses of interneurons with respect to the frequency of persistent rhythms, and the crucial dependence on gap-junction-mediated intercellular communication for the generation and maintenance of these rhythms.

Animals↗
PubMed1992

Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. II. N1 interneurons make cholinergic synapses with feeding motoneurons.

The N1 neurons are a population of interneurons active during the protraction phase of the feeding rhythm. All the N1 neurons are coupled by electrical synapses which persist in a high Mg/low Ca saline which blocks chemical synapses. Individual N1 spikes produce discrete electrotonic postsynaptic potentials (PSPS) in other N1 cells, but the coupling is not strong enough to ensure 1:1 firing. Bursts of N1 spikes generate compound PSPS in the feeding motoneurons. The sign (excitation or inhibition) of the N1 input corresponds with the synaptic barrage recorded during the protraction phase. Discrete PSPS are only resolved in a Hi-Di saline. Their variation in latency and number can be explained by variation in electrotonic propagation within the electrically coupled network of N1 cells. The excitatory postsynaptic potentials (ESPS) in the 1 cell are reduced by 0.5 mM antagonists hexamethonium (HMT), atropine (ATR), curare (d-TC) and by methylxylocholine (MeXCh), all of which block the excitatory cholinergic receptor (Elliott et al. (Phil. Trans. R. Soc. Lond. 336, 157-166 (Preceding paper.) (1992)). The 1 cell EPSPS were transiently blocked by phenyltrimethylammonium (PTMA), which is both an agonist and antagonist at the 1 cell excitatory acetylcholine (ACh) receptor (Elliott et al. 1992). The inhibitory postsynaptic potential (IPSP) in the 3 cell is blocked by bath applications of MeXCh and PTMA, which both abolish the response of the 3 cell to ACh (Elliott et. al. 1992). The effects of the cholinergic antagonists on the response of 4 cluster and 5 cells to N1 stimulation matches their response to ACh (Elliott et al. 1992). It is concluded that the population of N1 cells are multiaction, premotor cholinergic interneurons.

Acetylcholine↗
PubMed1991

Interneurones of the lumbar cord related to spontaneous locomotor activity in the rabbit. I. Rhythmically active interneurones.

In decorticate, unanaesthetized and curarized rabbit preparations displaying spontaneous fictive locomotor sequences, the firing pattern of neurones was recorded extracellularly in the L6-S1 spinal cord. These neurones, located in the intermediate part of the cord, were not invaded by antidromic stimulation of the hindlimb muscle nerves and thus were considered as interneurones (or propriospinal or tract cells ascending to the brain). When compared to the output from the ipsilateral muscle nerves, these neurones were classified as flexor (F INs) or extensor (E INs) according to the phase of the locomotor cycle when they displayed their maximal firing rate. Among 69 F INs, 33 maintained tonic firing during the periods between episodes of locomotor activity. Their maximal firing rate was in phase with the flexor efferent bursts of the locomotor sequence; during the extensor phase, they maintained an instantaneous frequency (i.f.) that was clearly above the resting i.f. Of these neurones, six became completely silent during the initial flexorextensor coactivation that opened the sequence (F1 neurones) whereas the 27 others increased their firing rate at that time (F2 neurones). The other neurones (36 F3) were silent between the locomotor episodes. Although most of them had a rhythmic activity limited to the flexor bursts, some fired throughout locomotor sequence with a maximal rate during flexor bursts. All the 123 E neurones completely stopped firing during the flexor phase. As was the case for F3 neurone firing, E3 neurone firing (34 neurones) occurred only during periods of locomotor activity. Among the neurones that displayed tonic activity between locomotor episodes, the E2 neurones (24 from 123) remained at this resting value during the extensor phase whereas the E1 neurones (65 neurones) showed an increased i.f. for all or part of this phase. These data, which suggest an asymmetrical genesis of the flexor and extensor activities in locomotion, need to be supported by further analysis.

Animals↗
PubMed2001

Activation and reconfiguration of fictive feeding by the octopamine-containing modulatory OC interneurons in the snail Lymnaea.

We describe the role of the octopamine-containing OC interneurons in the buccal feeding system of Lymnaea stagnalis. OC neurons are swallowing phase interneurons receiving inhibitory inputs in the N1 and N2 phases, and excitatory inputs in the N3 phase of fictive feeding. Although the OC neurons do not always fire during feeding, the feeding rate is significantly (P < 0.001) higher when both SO and OC fire in each cycle than when only the SO fires. In 28% of silent preparations, a single stimulation of an OC interneuron evokes the feeding pattern. Repetitive stimulation of the OC interneuron increases the proportion of responsive preparations to 41%. The OC interneuron not only changes both the feeding rate and reconfigures the pattern. Depolarization of the OC interneurons increases the feeding rate and removes the B3 motor neuron from the firing sequence. Hyperpolarization slows it down (increasing the duration of N1 and N3 phases) and recruits the B3 motor neuron. OC interneurons form synaptic connections onto buccal motor neurons and interneurons but not onto the cerebral (cerebral giant cell) modulatory neurons. OC interneurons are electrically coupled to all N3 phase (B4, B4Cl, B8) feeding motor neurons. They form symmetrical connections with the N3p interneurons having dual electrical (excitatory) and chemical (inhibitory) components. OC interneurons evoke biphasic synaptic inputs on the protraction phase interneurons (SO, N1L, N1M), with a short inhibition followed by a longer lasting depolarization. N2d interneurons are hyperpolarized, while N2v interneurons are slowly depolarized and often fire a burst after OC stimulation. Most motor neurons also receive synaptic responses from the OC interneurons. Although OC and N3p interneurons are both swallowing phase interneurons, their synaptic contacts onto follower neurons are usually different (e.g., the B3 motor neurons are inhibited by OC, but excited by N3p interneurons). Repetitive stimulation of OC interneuron facilitates the excitatory component of the biphasic responses evoked on the SO, N1L, and N1M interneurons, but neither the N2 nor the N3 phase interneurons display a similar longer-lasting excitatory effect. OC interneurons are inhibited by all the buccal feeding interneurons, but excited by the serotonergic modulatory CGC neurons. We conclude that OC interneurons are a new kind of swallowing phase interneurons. Their connections with the buccal feeding interneurons can account for their modulatory effects on the feeding rhythm. As they contain octopamine, this is the first example in Lymnaea that monoaminergic modulation and reconfiguration are provided by an intrinsic member of the buccal feeding network.

Action Potentials↗
PubMed1999

GABAergic and non-GABAergic spiking interneurons of local and intersegmental groups in the crayfish terminal abdominal ganglion.

In the first step toward identifying the neurotransmitter released from spiking interneurons of both local and intersegmental groups in the crayfish terminal abdominal ganglion, the authors examined whether spiking local interneurons and ascending intersegmental interneurons contain the transmitter gamma-aminobutyric acid (GABA). In this paper, 17 identified ascending interneurons and three spiking local interneurons were stained by intracellular injection of Lucifer yellow and subsequently treated for immunocytochemical staining against GABA. Double-labeling experiments revealed that six identified ascending interneurons are GABAergic, but no spiking local interneurons show GABA-like immunoreactivity. Four ascending interneurons with GABA-like immunoreactivity (reciprocal closing ascending neuron 5 [RC-5], reciprocal opening ascending neuron 6 [RO-6], variable-effect ascending interneuron 1 [VE-1], and no-effect ascending interneuron 4[NE-4]) had cell bodies that formed a cluster on the ventral surface of the rostral edge of the ganglion, whereas two GABAergic interneurons (coinhibiting ascending interneuron 2 [CI-2] and NE-2) had cell bodies in a caudal region around the cell body of the seventh flexor inhibitor (FI) motor neuron. Another four rostral interneurons (RC-2, RC-3, RC-4, and NE-3) and seven caudal interneurons (CI-3, RC-7, RO-1, RO-2, RO-3, RO-4, and NE-1) had no GABA-like immunoreactivity. Because VE-1 is known to make direct inhibitory connections with other ascending interneurons, whereas RC-3 and RO-1 are known to make direct excitatory connections, the immunocytochemical results from this study are consistent with previous physiological studies. Although many spiking local interneurons (including spiking local interneuron 1 of the anterior group [sp-ant1]) made direct inhibitory connections with nonspiking local interneurons, three spiking local interneurons (sp-ant1, spiking local interneuron 6 of the medial group [sp-med6], and spiking interneuron 5 of the posterior group [sp-post]) do not show GABA-like immunoreactivity. These results suggest that the inhibitory transmitter released from spiking local interneurons is not GABA but that another substance mediates the inhibitory action of these interneurons. J. Comp. Neurol. 410:677-688.

Action Potentials↗