Biomedical subjects

Bruce A Carlson

Publications and source records attributed to Bruce A Carlson.

8 recordsLinked to original sources

PubMed2006

Stimulus selectivity is enhanced by voltage-dependent conductances in combination-sensitive neurons.

Central sensory neurons often respond selectively to particular combinations of stimulus attributes, but we know little about the underlying cellular mechanisms. The weakly electric fish Gymnarchus discriminates the sign of the frequency difference (Df) between a neighbor's electric organ discharge (EOD) and its own EOD by comparing temporal patterns of amplitude modulation (AM) and phase modulation (PM). Sign-selective neurons in the midbrain respond preferentially to either positive frequency differences (Df >0 selective) or negative frequency differences (Df <0 selective). To study the mechanisms of combination sensitivity, we made whole cell intracellular recordings from sign-selective midbrain neurons in vivo and recorded postsynaptic potential (PSP) responses to AM, PM, Df >0, and Df <0. Responses to AM and PM consisted of alternating excitatory and inhibitory PSPs. These alternating responses were in phase for the preferred sign of Df and offset for the nonpreferred sign of Df. Therefore a certain degree of sign selectivity was predicted by a linear sum of the responses to AM and PM. Responses to the nonpreferred sign of Df, but not the preferred sign of Df, were substantially weaker than linear predictions, causing a significant increase in the actual degree of sign selectivity. By using various levels of current clamp and comparing our results to simple models of synaptic integration, we demonstrate that this decreased response to the nonpreferred sign of Df is caused by a reduction in voltage-dependent excitatory conductances. This finding reveals that nonlinear decoders, in the form of voltage-dependent conductances, can enhance the selectivity of single neurons for particular combinations of stimulus attributes.

Algorithms↗

PubMed2006

Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes.

Accurate sensory perception often depends on the independent encoding and subsequent integration of multiple stimulus attributes. In the weakly electric fish Eigenmannia, P- and T-type primary afferent fibers are specialized for encoding the amplitude and phase, respectively, of electrosensory stimuli. We used a stimulus estimation technique to quantify the ability of P- and T-units to encode random modulations in amplitude and phase. As expected, P-units exhibited a clear preference for encoding amplitude modulations, whereas T-units exhibited a clear preference for encoding phase modulations. Surprisingly, both types of afferents also encoded their nonpreferred stimulus attribute when it was presented in isolation or when the preferred stimulus attribute was sufficiently weak. Because afferent activity can be affected by modulations in either amplitude or phase, it is not possible to unambiguously distinguish between these two stimulus attributes by observing the activity of a single afferent fiber. Simple model neurons with a preference for encoding either amplitude or phase also encoded their nonpreferred stimulus attribute when it was presented in isolation, suggesting that such ambiguity is unavoidable. Using the well known jamming avoidance response as a probe of electrosensory perception, we show that the ambiguity at the single-neuron level gives rise to a systematic misrepresentation of stimuli at the population level and a resulting misperception of the amplitude and phase of electrosensory stimuli.

Action Potentials↗

PubMed2005

Electric organ discharge patterns during group hunting by a mormyrid fish.

Weakly electric fish emit and receive low-voltage electric organ discharges (EODs) for electrolocation and communication. Since the discovery of the electric sense, their behaviours in the wild have remained elusive owing to their nocturnal habits and the inaccessible environments in which they live. The transparency of Lake Malawi provided the first opportunity to simultaneously observe freely behaving mormyrid fish and record their EODs. We observed a piscivorous mormyrid, Mormyrops anguilloides, hunting in small groups in Lake Malawi while feeding on rock-frequenting cichlids of the largest known vertebrate species flock. Video recordings yielded the novel and unexpected finding that these groups resembled hunting packs by being largely composed of the same individuals across days. We show that EOD accelerations accompany prey probing and size estimation by M. anguilloides. In addition, group members occasionally synchronize bursts of EODs with an extraordinary degree of precision afforded by the mormyrid echo response. The characteristics and context of burst synchronization suggest that it may function as a pack cohesion signal. Our observations highlight the potential richness of social behaviours in a basal vertebrate lineage, and provide a framework for future investigations of the neural mechanisms, behavioural rules and ecological significance of social predation in M. anguilloides.

Action Potentials↗

PubMed2004

Nonlinear response properties of combination-sensitive electrosensory neurons in the midbrain of Gymnarchus niloticus.

The jamming avoidance response of the weakly electric fish Gymnarchus niloticus relies on determining the sign of the frequency difference (Df) between the fish's own electric organ discharge (EOD) and that of a neighbor, which is achieved by comparing modulations in amplitude (AM) and phase (PM) that result from the summation of their EODs. These two stimulus features are processed in separate pathways that converge in the torus semicircularis on combination-sensitive neurons, many of which are selective for the sign of Df. We recorded extracellular single-unit responses to independent stimulation with AM and PM and combined AM-PM stimulation to determine how sign selectivity is established. Responses to AM and PM frequently summated nonlinearly, leading to sign-selective responses as a result of facilitation to the preferred sign of Df and/or suppression to the nonpreferred sign of Df. Facilitation typically occurred when responses to AM and PM were aligned, whereas suppression typically occurred when they were offset. By experimentally manipulating the degree of alignment between these two responses, we found that the summed response was dependent on their relative timing. In addition, we found a unique class of units that were sensitive to differences in amplitude between two body surfaces. This sensitivity rendered such units immune to the problem of orientation ambiguity, in which the sign selectivity of a single neuron reverses with changes in stimulus orientation. We discuss potential synaptic mechanisms for driving nonlinear responses in these and other combination-sensitive neurons.

Animal Communication↗

PubMed2004

Central control of electric signaling behavior in the mormyrid Brienomyrus brachyistius: segregation of behavior-specific inputs and the role of modifiable recurrent inhibition.

Like all mormyrid fish, Brienomyrus brachyistius produces an electric organ discharge (EOD) with a constant waveform and variable sequence of pulse intervals (SPI). Periodic bursts fall into two display categories termed 'scallops' and 'accelerations', with a third category termed 'rasps' that appears to combine the two. The medullary EOD command nucleus (CN) receives excitatory input from the midbrain precommand nucleus (PCN) and the thalamic dorsal posterior nucleus (DP), both of which are regulated by a recurrent inhibitory projection from the ventroposterior nucleus of the torus semicircularis (VP). We tested the following hypotheses: (1) PCN and DP are responsible for generating different burst types (scallops and accelerations, respectively), (2) differences in the strength of recurrent inhibition are related to physiological differences between PCN and DP and (3) recurrent inhibition regulates the resting electromotor rhythm, while disinhibition releases PCN and DP, allowing them to generate bursts. Iontophoresis of the excitatory neurotransmitter L-glutamate (L-Glu) into DP led to acceleration-like output patterns, while in PCN it led to scallop-like output patterns. Iontophoresis of the inhibitory neurotransmitter gamma-amino-butyric acid (GABA) into DP and PCN led to an elongation of intervals, as did iontophoresis of L-Glu into VP. Iontophoresis of the GABA(A) receptor blocker bicuculline methiodide (BMI) into DP and PCN induced repetitive bursting behavior and eliminated differences in the effects of L-Glu iontophoresis in the two nuclei. These results support our three hypotheses, suggesting that production of different communication behaviors may be regulated by spatially distinct groups of neurons, and recurrent inhibition and disinhibition may play an active role in driving and shaping such behaviors.

Animal Communication↗

PubMed2003

Single-unit activity patterns in nuclei that control the electromotor command nucleus during spontaneous electric signal production in the mormyrid Brienomyrus brachyistius.

Mormyrid fish generate weak electric organ discharges (EODs) used for communication and navigation. EODs are initiated in the medullary command nucleus (CN), which receives dense projections from the mesencephalic precommand nucleus (PCN) and the adjacent thalamic dorsal posterior nucleus (DP), plus a minor projection from the ventral edge of the toral ventroposterior nucleus (VPv). The dorsal region of the ventroposterior nucleus (VPd) projects to DP-PCN and receives input from the electric organ corollary discharge pathway. I recorded extracellularly from single units within DP-PCN and VPd and correlated their activity patterns with electromotor output to generate hypotheses on electromotor control mechanisms. DP-PCN neurons show an oscillatory pattern of activity, firing within a window of 10-200 msec before each EOD, while remaining silent for 50-150 msec after each EOD. VPd neurons only fire during the silent period of DP-PCN neurons, suggesting that they provide recurrent inhibition to DP-PCN. During "scallops", only DP-PCN neurons with high baseline firing rates increase their activity, whereas during "accelerations", only neurons with low baseline firing rates show a strong increase in activity. Thus, the generation of different displays likely results from the activation of different groups of neurons projecting to CN. The activity of VPd neurons decreases during both displays, suggesting that disinhibition plays an important role in their generation. The mormyrid electromotor network shares many functional properties with central pattern generators (CPGs) found in relatively simple motor systems, indicating that it may be an excellent model system for studying CPG function in vertebrate communication.

Action Potentials↗

PubMed2002

Neuroanatomy of the mormyrid electromotor control system.

Mormyrid fish produce a diverse range of electric signals that are under the control of a central electromotor network. The anatomical organization of this network was delineated by injecting biotinylated compounds into neurophysiologically identified nuclei. Previous work using retrograde labeling with horseradish peroxidase indicated that the medullary command nucleus (CN) receives inputs from the precommand nucleus (PCN) at the mesencephalic-diencephalic border and the ventroposterior nucleus (VP) in the torus semicircularis. This study confirms these projections and identifies the dorsal posterior nucleus (DP) in the thalamus as an additional input to CN. DP and PCN form a bilateral column of cells extending ventrolaterally and caudally from the dorsal thalamus. The primary input to DP/PCN is from VP, which is identified as having two distinct subdivisions. A small group of large, multipolar cells along the ventral edge projects to DP/PCN and to CN, whereas a dorsal group of small, ovoid cells projects to DP/PCN but not to CN. VP receives input from the tectum mesencephali and the mesencephalic command-associated nucleus (MCA). As in all vertebrates, the tectum mesencephali receives input from several sources and likely provides multimodal sensory input to the electromotor system. MCA is part of the electromotor corollary discharge pathway, and its projection to VP suggests a feedback loop. These results, combined with recent physiological studies and comparisons with other taxa, suggest that modifiable feedback to DP/PCN plays a critical role in electromotor control and that the different inputs to CN may each be responsible for generating distinct electric signals.

Animals↗

PubMedDate not supplied

Electric signaling behavior and the mechanisms of electric organ discharge production in mormyrid fish.

Mormyrid fish communicate and navigate using electric organ discharges (EODs). The EOD is highly stereotyped and provides information on sender identity, including species, sex, reproductive condition, and possibly relative status and individual identity. By contrast, the sequence of pulse intervals (SPI) is variable and plays more of a role in signaling behavioral states. Various types of SPI displays may be produced, including tonic patterns such as 'random' and 'regularized', and phasic patterns such as 'bursts' and cessations'. Certain displays have been linked to specific behaviors such as aggression, submission, courtship and active exploration. In addition, interacting pairs of fish may produce stereotyped displays involving the relative timing of their EODs. The EOD waveform is controlled by the morphological and physiological properties of cells in the electric organ termed electrocytes. Differences in the innervation, morphology, size and membrane characteristics of electrocytes have been directly linked to species and sex differences in the EOD. The generation of each EOD is initiated in the medullary command nucleus (CN), which thereby determines the timing of EOD output. CN does not have any properties of a pacemaker, but rather appears to integrate descending inputs that affect the probability of EOD production. The precommand nucleus (PCN) provides a major source of excitatory input to CN and is itself inhibited by corollary discharge feedback following the production of each EOD. Changes in the activity of PCN and its inhibitory feedback neurons modify EOD output, and therefore drive the generation of SPI patterns. Current studies are addressing the mechanisms underlying the generation of these patterns and preliminary results suggest that different types of signals may be controlled by distinct components of the electromotor system. This is similar to findings in other electrogenic teleosts, suggesting that it may be a general feature in the motor control of signaling behavior.

Action Potentials↗