Continual Learning in a Multi-Layer Network of an Electric Fish.

Distributing learning across multiple layers has proven extremely powerful in artificial neural networks. However, little is known about how multi-layer learning is implemented in the brain. Here, we provide an account of learning across multiple processing layers in the electrosensory lobe (ELL) of mormyrid fish and report how it solves problems well known from machine learning. Because the ELL operates and learns continuously, it must reconcile learning and signaling functions without switching its mode of operation. We show that this is accomplished through a functional compartmentalization within intermediate layer neurons in which inputs driving learning differentially affect dendritic and axonal spikes. We also find that connectivity based on learning rather than sensory response selectivity assures that plasticity at synapses onto intermediate-layer neurons is matched to the requirements of output neurons. The mechanisms we uncover have relevance to learning in the cerebellum, hippocampus, and cerebral cortex, as well as in artificial systems.

The morphology and evolution of chondrichthyan cranial muscles: A digital dissection of the elephantfish Callorhinchus milii and the catshark Scyliorhinus canicula.

The anatomy of sharks, rays, and chimaeras (chondrichthyans) is crucial to understanding the evolution of the cranial system in vertebrates due to their position as the sister group to bony fishes (osteichthyans). Strikingly different arrangements of the head in the two constituent chondrichthyan groups-holocephalans and elasmobranchs-have played a pivotal role in the formation of evolutionary hypotheses targeting major cranial structures such as the jaws and pharynx. However, despite the advent of digital dissections as a means of easily visualizing and sharing the results of anatomical studies in three dimensions, information on the musculoskeletal systems of the chondrichthyan head remains largely limited to traditional accounts, many of which are at least a century old. Here, we use synchrotron tomographic data to carry out a digital dissection of a holocephalan and an elasmobranch widely used as model species: the elephantfish, Callorhinchus milii, and the small-spotted catshark, Scyliorhinus canicula. We describe and figure the skeletal anatomy of the head, labial, mandibular, hyoid, and branchial cartilages in both taxa as well as the muscles of the head and pharynx. In Callorhinchus, we make several new observations regarding the branchial musculature, revealing several previously unreported or ambiguously characterized muscles, likely homologous to their counterparts in the elasmobranch pharynx. We also identify a previously unreported structure linking the pharyngohyal of Callorhinchus to the neurocranium. Finally, we review what is known about the evolution of chondrichthyan cranial muscles from their fossil record and discuss the implications for muscle homology and evolution, broadly concluding that the holocephalan pharynx is likely derived from a more elasmobranch-like form which is plesiomorphic for the chondrichthyan crown group. This dataset has great potential as a resource, particularly for researchers using these model species for zoological research, functional morphologists requiring models of musculature and skeletons, as well as for palaeontologists seeking comparative models for extinct taxa.

Hidden species diversity in Marcusenius moorii (Teleostei: Mormyridae) from the Congo Basin.

New collections from the Yangambi Biosphere Reserve (YBR) and Okapi Wildlife Reserve (OWR) revealed the presence of two groups of specimens similar to, but different from Marcusenius moorii. To study both these groups, an integrated morphological and genetic (mtDNA, cytb) approach was used. This study revealed that one of the two groups is conspecific with Marcusenius lambouri, a junior synonym of M. moorii, which is herein revalidated, with M. moorii longulus as its junior synonym. Marcusenius lambouri differs from M. moorii by a higher number of lateral line scales (44-46 vs. 40-43), a shorter pectoral-fin length (14.6-19.9 vs. 20.3-25.2% standard length; LS ) and a more elongated body due to a usually shallower middle body depth (19.8-26.5 vs. 26.3-35.9% LS ). The other group revealed to be a new species for science, Marcusenius verheyenorum, which can be distinguished from its congeners with eight circumpeduncular scales by the following unique combination of characters: a rounded head with a terminal mouth; a short and deep caudal peduncle (middle caudal-peduncle depth, 44.9-54.6% caudal-peduncle length; LCP ), a deep body (middle body depth, 27.7-34.2% LS ), 38-43 scales on the lateral line, 40-41 vertebrae, 20-21 dorsal-fin rays and 26 anal-fin rays. Some specimens previously attributed to M. moorii were examined and reassigned to M. lambouri or M. verheyenorum. As a result, M. moorii and M. lambouri occur in sympatry in the middle Congo Basin, with the distribution area of M. moorii still further extending into the lower Congo Basin. Instead, the distribution of M. verheyenorum is limited to some right bank tributaries of the upstream part of the middle Congo Basin. Two museum records from the Lilanda River (YBR), collected in the 1950s and previously identified as M. moorii, were re-identified as belonging to the new species, M. verheyenorum. However, the species now seems locally extinct in that region, which reflects the significant anthropogenic effects even within this reserve.

The Cyphomyrus Myers 1960 (Osteoglossiformes: Mormyridae) of the Lufira basin (Upper Lualaba: DR Congo): A generic reassignment and the description of a new species.

Within a comparative morphological framework, Hippopotamyrus aelsbroecki, only known from the holotype originating from Lubumbashi, most probably the Lubumbashi River, a left bank subaffluent of the Luapula River, is reallocated to the genus Cyphomyrus. This transfer is motivated by the fact that H. aelsbroecki possesses a rounded or vaulted predorsal profile, an insertion of the dorsal fin far anterior to the level of the insertion of the anal fin, and a compact, laterally compressed and deep body. In addition, a new species of Cyphomyrus is described from the Lufira basin, Cyphomyrus lufirae. Cyphomyrus lufirae was collected in large parts of the Middle Lufira, upstream of the Kyubo Falls and just downstream of these falls in the lower Lufira and its nearby left bank affluent, the Luvilombo River. The new species is distinguished from all its congeners, that is, firstly, from C. aelsbroecki, C. cubangoensis and C. discorhynchus, by a low number of dorsal fin rays, 27-32 (vs. higher, 36 (37), 34 (33-41) an 38 (38-40), respectively) and, secondly, from C. aelsbroecki, C. cubangoensis, and C. discorhynchus by a large prepelvic distance, 41.0-43.8% LS (vs. shorter, 39.7%, 38.9-39.1% and 37.0-41.0% LS , respectively). The description of yet another new species for the Upemba National Park and the Kundelungu National Park further highlights their importance for fish protection and conservation in the area. Hence, there is an urgent need for the full integration of fish into the management plans of these parks.

A shocking discovery of threat risks on newly described species of weakly electric fishes.

This study aims to investigate relationships between species traits and publication date in the weakly electric osteoglossiform Mormyroidea (African knifefish and elephantfishes) and the ostariophysan Gymnotiformes (Neotropical knifefishes). It is investigated whether body size and geographic distribution area are correlated with publication date and whether extinction risk differs between both phylogenetically distant and geographically isolated clades. Statistical modelling indicates that the number of new species described annually is stable in mormyroids and clearly increasing in gymnotiforms. Best-fitting generalised linear models (GLM) indicate that the newly discovered species are more often of small-bodied, predominantly narrowly distributed and more likely to be threatened with extinction. These characteristics are more pronounced in mormyroids when compared with gymnotiforms, suggesting that some African electric fishes may live an ephemeral existence after formal description. Despite taxonomic work has been more intense in the Neotropics than in Africa in the recent decades, there is evidence that the African continent represents the next frontier of species descriptions. Taxonomic studies are fundamental for the understanding of richness and distribution and hence extinction risk assessment and conservation, of these remarkable convergent fish clades.

Intraspecific Energetic Trade-Offs and Costs of Encephalization Vary from Interspecific Relationships in Three Species of Mormyrid Electric Fishes.

The evolution of increased encephalization comes with an energetic cost. Across species, this cost may be paid for by an increase in metabolic rate or by energetic trade-offs between the brain and other energy-expensive tissues. However, it remains unclear whether these solutions to deal with the energetic requirements of an enlarged brain are related to direct physiological constraints or other evolved co-adaptations. We studied the highly encephalized mormyrid fishes, which have extensive species diversity in relative brain size. We previously found a correlation between resting metabolic rate and relative brain size across species; however, it is unknown how this interspecific relationship evolved. To address this issue, we measured intraspecific variation in relative brain size, the sizes of other organs, metabolic rate, and hypoxia tolerance to determine if intraspecific relationships between brain size and organismal energetics are similar to interspecific relationships. We found that 3 species of mormyrids with varying degrees of encephalization had no intraspecific relationships between relative brain size and relative metabolic rate or relative sizes of other organs, and only 1 species had a relationship between relative brain size and hypoxia tolerance. These species-specific differences suggest that the interspecific relationship between metabolic rate and relative brain size is not the result of direct physiological constraints or strong stabilizing selection, but is instead due to other species level co-adaptations. We conclude that variation within species must be considered when determining the energetic costs and trade-offs underlying the evolution of extreme encephalization.

Growth-band counts from elephantfish Callorhinchus milii fin spines do not correspond with independently estimated ages.

Fin spines from elephantfish Callorhinchus milii were sectioned and viewed with transmitted white light under a compound microscope. The sections displayed growth bands but their interpretation and significance were unclear. Three different methods were used for counting growth bands. The results were compared with reference growth curves based on length-at-age estimates for six juvenile year classes derived from length-frequency distributions, and tagging data that showed longevity is at least 20 years. None of the three ageing methods showed good correspondence with the reference curves and all methods departed markedly from the reference curves at ages above 2 years old. Therefore, growth bands present in C. milii spines are not useful for ageing, at least with the three methods tested here. Spine bands may not represent age marks, but instead may be layers of material deposited irregularly to strengthen the spine.

Sensory Specializations of Mormyrid Fish Are Associated with Species Differences in Electric Signal Localization Behavior.

The ability to localize communication signals plays a fundamental role in social interactions. For signal localization to take place, the sensory system of the receiver must extract information about distance and direction to the sender from physical characteristics of the signal. In many sensory systems, information from multiple peripheral receptors must be integrated by central sensory pathways to determine the sender location. Here, we asked whether evolutionary divergence in the electrosensory and visual systems of mormyrid fish is associated with signal localization behavior. In mormyrids, differences in the distribution of electroreceptors on the surface of the skin are associated with differences in the midbrain exterolateral nucleus (EL). Species with electroreceptors clustered in three rosettes on both sides of the head have a small and undifferentiated EL. In contrast, EL is enlarged and subdivided into anterior (ELa) and posterior (ELp) regions in species that have electroreceptors broadly -distributed throughout the body. Interestingly, species with EL and clustered electroreceptors also have larger visual systems and higher visual acuity than species with ELa/ELp and broadly distributed electroreceptors. Species with broadly distributed electroreceptors and ELa/ELp approached a simulated conspecific by following the curved electric field lines generated by the electrosensory stimulus. In contrast, a species with small EL and clustered electroreceptors, but an enlarged visual system, followed shorter and straighter paths to the stimulus source. In the central electrosensory system, evoked field potentials in response to stimuli delivered from the left versus the right differed more in EL than in ELa/ELp. Our results suggest that signal localization behavior is associated with differences in sensory specializations. We propose that the distribution of electroreceptors on the body affects the ability of individuals to align parallel to electric field lines and maintain such alignment while approaching the signal source. The spatial resolution of sensory information relayed from the periphery to the midbrain in species with clustered electroreceptors may allow for gross, but not fine, processing of sender location. Furthermore, visual information may play an important role in localizing signaling individuals in species with small EL and clustered electroreceptors. In line with previous studies, we suggest that the physiological and behavioral differences associated with signal localization reflect adaptations to different habitats and social environments.

Anal-fin ray morphology indicates sexual maturity in Brevimyrus niger (Teleostei, Mormyridae).

This osteological survey of 249 specimens of Brevimyrus niger ranging in size from 44 to 137 mm standard length (LS ) demonstrated that developmental changes in anal-fin morphology can serve as a predictor of sexual maturity in this species. Anal-fin ray bases begin to expand when fish reach c. 90 mm LS at which size and above there were roughly equal numbers of individuals observed with expanded and unmodified anal-fin bases, reflecting a 1:1 sex ratio.

Androgen-induced pseudo-hermaphroditic phenotypes in female Brevimyrus niger Günther 1866 (Teleostei, Mormyridae).

This paper explores the plasticity of sexually dimorphic characters in subadult female Brevimyrus niger, an African weakly electric mormyrid species. Thirty-five fish were exposed in a staggered fashion (five fish a week) to aromatizable 17α-methyltestosterone over a period of 7 weeks; 18 fish served as untreated controls. 17α-MT induced precocious vitellogenesis that mirrored the natural maturational process during seasonal ovarian recrudescence. At the same time, 17α-MT exposure resulted in complete masculinization of the females' anal fin support structure normally observed during rainy season in adult males. We discuss possible hormonal mechanisms acting along the brain-pituitary-gonad axis that would explain the occurrence of precocious vitellogenesis and the male-typical transformation of the female's anal fin ray bases. Our findings are relevant to commercial aquaculture as the use of 17α-MT in fish hatcheries can pose serious environmental issues.

The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes.

A large brain can offer several cognitive advantages. However, brain tissue has an especially high metabolic rate. Thus, evolving an enlarged brain requires either a decrease in other energetic requirements, or an increase in overall energy consumption. Previous studies have found conflicting evidence for these hypotheses, leaving the metabolic costs and constraints in the evolution of increased encephalization unclear. Mormyrid electric fishes have extreme encephalization comparable to that of primates. Here, we show that brain size varies widely among mormyrid species, and that there is little evidence for a trade-off with organ size, but instead a correlation between brain size and resting oxygen consumption rate. Additionally, we show that increased brain size correlates with decreased hypoxia tolerance. Our data thus provide a non-mammalian example of extreme encephalization that is accommodated by an increase in overall energy consumption. Previous studies have found energetic trade-offs with variation in brain size in taxa that have not experienced extreme encephalization comparable with that of primates and mormyrids. Therefore, we suggest that energetic trade-offs can only explain the evolution of moderate increases in brain size, and that the energetic requirements of extreme encephalization may necessitate increased overall energy investment.

Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes.

Sensory systems play a key role in social behavior by mediating the detection and analysis of communication signals. In mormyrid fishes, electric signals are processed within a dedicated sensory pathway, providing a unique opportunity to relate sensory biology to social behavior. Evolutionary changes within this pathway led to new perceptual abilities that have been linked to increased rates of signal evolution and species diversification in a lineage called 'clade A'. Previous field observations suggest that clade-A species tend to be solitary and territorial, whereas non-clade-A species tend to be clustered in high densities suggestive of schooling or shoaling. To explore behavioral differences between species in these lineages in greater detail, I studied population densities, social interactions, and electric signaling in two mormyrid species, Gnathonemus victoriae (clade A) and Petrocephalus degeni (non-clade A), from Lwamunda Swamp, Uganda. Petrocephalus degeni was found at higher population densities, but intraspecific diversity in electric signal waveform was greater in G. victoriae. In the laboratory, G. victoriae exhibited strong shelter-seeking behavior and competition for shelter, whereas P. degeni were more likely to abandon shelter in the presence of conspecifics as well as electric mimics of signaling conspecifics. In other words, P. degeni exhibited social affiliation whereas G. victoriae exhibited social competition. Further, P. degeni showed correlated electric signaling behavior whereas G. victoriae showed anti-correlated signaling behavior. These findings extend previous reports of social spacing, territoriality, and habitat preference among mormyrid species, suggesting that evolutionary divergence in electrosensory processing relates to differences in social behavior.

Morphological and molecular investigations of the holocephalan elephant fish nephron: the existence of a countercurrent-like configuration and two separate diluting segments in the distal tubule.

In marine cartilaginous fish, reabsorption of filtered urea by the kidney is essential for retaining a large amount of urea in their body. However, the mechanism for urea reabsorption is poorly understood due to the complexity of the kidney. To address this problem, we focused on elephant fish (Callorhinchus milii) for which a genome database is available, and conducted molecular mapping of membrane transporters along the different segments of the nephron. Basically, the nephron architecture of elephant fish was similar to that described for elasmobranch nephrons, but some unique features were observed. The late distal tubule (LDT), which corresponded to the fourth loop of the nephron, ran straight near the renal corpuscle, while it was convoluted around the tip of the loop. The ascending and descending limbs of the straight portion were closely apposed to each other and were arranged in a countercurrent fashion. The convoluted portion of LDT was tightly packed and enveloped by the larger convolution of the second loop that originated from the same renal corpuscle. In situ hybridization analysis demonstrated that co-localization of Na(+),K(+),2Cl(-) cotransporter 2 and Na(+)/K(+)-ATPase α1 subunit was observed in the early distal tubule and the posterior part of LDT, indicating the existence of two separate diluting segments. The diluting segments most likely facilitate NaCl absorption and thereby water reabsorption to elevate urea concentration in the filtrate, and subsequently contribute to efficient urea reabsorption in the final segment of the nephron, the collecting tubule, where urea transporter-1 was intensely localized.

Comparative histology of the adult electric organ among four species of the genus Campylomormyrus (Teleostei: Mormyridae).

The electric organ (EO) of weakly electric mormyrids consists of flat, disk-shaped electrocytes with distinct anterior and posterior faces. There are multiple species-characteristic patterns in the geometry of the electrocytes and their innervation. To further correlate electric organ discharge (EOD) with EO anatomy, we examined four species of the mormyrid genus Campylomormyrus possessing clearly distinct EODs. In C. compressirostris, C. numenius, and C. tshokwe, all of which display biphasic EODs, the posterior face of the electrocytes forms evaginations merging to a stalk system receiving the innervation. In C. tamandua that emits a triphasic EOD, the small stalks of the electrocyte penetrate the electrocyte anteriorly before merging on the anterior side to receive the innervation. Additional differences in electrocyte anatomy among the former three species with the same EO geometry could be associated with further characteristics of their EODs. Furthermore, in C. numenius, ontogenetic changes in EO anatomy correlate with profound changes in the EOD. In the juvenile the anterior face of the electrocyte is smooth, whereas in the adult it exhibits pronounced surface foldings. This anatomical difference, together with disparities in the degree of stalk furcation, probably contributes to the about 12 times longer EOD in the adult.

Visual Capability of the Weakly Electric Fish Apteronotus albifrons as Revealed by a Modified Retinal Flat-Mount Method.

Apteronotus albifrons (Gymnotiformes, Apteronotidae) is well known to have a sophisticated active electrosense system and is commonly described as having poor vision or being almost blind. However, some studies on this species suggest that the visual system may have a role in sensing objects in the environment. In this study, we investigated the visual capabilities of A. albifrons by focusing on eye morphology and retinal ganglion cell distribution. The eyes were almost embedded below the body surface and pigmented dermal tissue covered the peripheral regions of the pupil, limiting the direction of incoming light. The lens was remarkably flattened compared to the almost spherical lenses of other teleosts. The layered structure of the retina was not well delineated and ganglion cells did not form a continuous sheet of cell bodies. A newly modified retinal flat-mount method was applied to reveal the ganglion cell distribution. This method involved postembedding removal of the pigment epithelium of the retina for easier visualization of ganglion cells in small and/or fragile retinal tissues. We found that ganglion cell densities were relatively high in the periphery and highest in the nasal and temporal retina, although specialization was not so high (approx. 3:1) with regard to the medionasal or mediotemporal axis. The estimated highest possible spatial resolving power was around 0.57 and 0.54 cycles/degree in the nasal and temporal retina, respectively, confirming the lower importance of the visual sense in this species. However, considering the hunting nature of A. albifrons, the relatively high acuity of the caudal visual field in combination with electrolocation may well be used to locate prey situated close to the side of the body.

Using a classic paper by Bell as a platform for discussing the role of corollary discharge-like signals in sensory perception and movement control.

Decades of behavioral observations have shown that invertebrate and vertebrate species have the ability to distinguish between self-generated afferent inputs versus those that are generated externally. In the present article, I describe activities focused around the discussion of a classic American Physiological Society paper by Curtis C. Bell that lays the foundation for students to investigate the neural substrate underlying this ability. Students will leave this activity being able to 1) describe the technical aspects and limitations of an electric fish preparation commonly used to acquire single unit (extracellular) neurophysiological data, 2) provide physiological evidence showing that the activity of principal cells in the posterior lateral line lobe of the electric fish brain reflects that of a reafference comparator that could be used in dissociating self-generated versus externally generated sensory signals, and 3) knowledgeably discuss hypotheses concerning the role of corollary discharge and cerebellar-like structures in vertebrate and invertebrate species. The skills and background knowledge gained in this activity lay the platform for advanced study of scientific investigations into sensory, motor, and cognitive processes in undergraduate, graduate, or medical school curricula.

Multiplexed temporal coding of electric communication signals in mormyrid fishes.

The coding of stimulus information into patterns of spike times occurs widely in sensory systems. Determining how temporally coded information is decoded by central neurons is essential to understanding how brains process sensory stimuli. Mormyrid weakly electric fishes are experts at time coding, making them an exemplary organism for addressing this question. Mormyrids generate brief, stereotyped electric pulses. Pulse waveform carries information about sender identity, and it is encoded into submillisecond-to-millisecond differences in spike timing between receptors. Mormyrids vary the time between pulses to communicate behavioral state, and these intervals are encoded into the sequence of interspike intervals within receptors. Thus, the responses of peripheral electroreceptors establish a temporally multiplexed code for communication signals, one consisting of spike timing differences between receptors and a second consisting of interspike intervals within receptors. These signals are processed in a dedicated sensory pathway, and recent studies have shed light on the mechanisms by which central circuits can extract behaviorally relevant information from multiplexed temporal codes. Evolutionary change in the anatomy of this pathway is related to differences in electrosensory perception, which appears to have influenced the diversification of electric signals and species. However, it remains unknown how this evolutionary change relates to differences in sensory coding schemes, neuronal circuitry and central sensory processing. The mormyrid electric communication pathway is a powerful model for integrating mechanistic studies of temporal coding with evolutionary studies of correlated differences in brain and behavior to investigate neural mechanisms for processing temporal codes.

Biomimetic and bio-inspired robotics in electric fish research.

Weakly electric knifefish have intrigued both biologists and engineers for decades with their unique electrosensory system and agile swimming mechanics. Study of these fish has resulted in models that illuminate the principles behind their electrosensory system and unique swimming abilities. These models have uncovered the mechanisms by which knifefish generate thrust for swimming forward and backward, hovering, and heaving dorsally using a ventral elongated median fin. Engineered active electrosensory models inspired by electric fish allow for close-range sensing in turbid waters where other sensing modalities fail. Artificial electrosense is capable of aiding navigation, detection and discrimination of objects, and mapping the environment, all tasks for which the fish use electrosense extensively. While robotic ribbon fin and artificial electrosense research has been pursued separately to reduce complications that arise when they are combined, electric fish have succeeded in their ecological niche through close coupling of their sensing and mechanical systems. Future integration of electrosense and ribbon fin technology into a knifefish robot should likewise result in a vehicle capable of navigating complex 3D geometries unreachable with current underwater vehicles, as well as provide insights into how to design mobile robots that integrate high bandwidth sensing with highly responsive multidirectional movement.

Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish.

Sensory neurons continually adapt their processing properties in response to changes in the sensory environment or the brain's internal state. Neuromodulators are thought to mediate such adaptation through a variety of receptors and their action has been implicated in processes such as attention, learning and memory, aggression, reproductive behaviour and state-dependent mechanisms. Here, we review recent work on neuromodulation of electrosensory processing by acetylcholine and serotonin in the weakly electric fish Apteronotus leptorhynchus. Specifically, our review focuses on how experimental application of these neuromodulators alters excitability and responses to sensory input of pyramidal cells within the hindbrain electrosensory lateral line lobe. We then discuss current hypotheses on the functional roles of these two neuromodulatory pathways in regulating electrosensory processing at the organismal level and the need for identifying the natural behavioural conditions that activate these pathways.

Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish.

While peripheral sensory neurons respond to natural stimuli with a broad range of spatiotemporal frequencies, central neurons instead respond sparsely to specific features in general. The nonlinear transformations leading to this emergent selectivity are not well understood. Here we characterized how the neural representation of stimuli changes across successive brain areas, using the electrosensory system of weakly electric fish as a model system. We found that midbrain torus semicircularis (TS) neurons were on average more selective in their responses than hindbrain electrosensory lateral line lobe (ELL) neurons. Further analysis revealed two categories of TS neurons: dense coding TS neurons that were ELL-like and sparse coding TS neurons that displayed selective responses. These neurons in general responded to preferred stimuli with few spikes and were mostly silent for other stimuli. We further investigated whether information about stimulus attributes was contained in the activities of ELL and TS neurons. To do so, we used a spike train metric to quantify how well stimuli could be discriminated based on spiking responses. We found that sparse coding TS neurons performed poorly even when their activities were combined compared with ELL and dense coding TS neurons. In contrast, combining the activities of as few as 12 dense coding TS neurons could lead to optimal discrimination. On the other hand, sparse coding TS neurons were better detectors of whether their preferred stimulus occurred compared with either dense coding TS or ELL neurons. Our results therefore suggest that the TS implements parallel detection and estimation of sensory input.