Neural Coding: Taking a close look at electrosensing

  1. Tatyana O Sharpee  Is a corresponding author
  1. Salk Institute for Biological Studies, United States

The question of how animals make sense of their environment is of interest in both neuroscience and computer science. The key challenge is to understand how to categorize events in ways that are useful to the animal, and also practical to implement. Typically, this involves separating information about an event (for example, what kind of object has just appeared in the animal's environment?) from information about where the event happened (DiCarlo et al., 2012).

While much of the research in this area has focused on vision, similar computational principles are involved for other senses, including smell and hearing (King and Nelken, 2009). In particular it is thought that the initial signal detected by sensory neurons in the peripheral regions of the brain undergoes a series of transformations as it is passed from one set of neurons to another. The end result is to produce an representation of the event (for example, the presence of another animal of a particular species) that does not depend on where the event happened. However, much remains to be understood about the transformations that would make this possible.

In this situation, studying species with exotic senses not used by humans might shed new light on the problem. Now, in eLife, Michael Metzen, Volker Hofmann and Maurice Chacron from McGill University report the results of experiments on fish called brown ghost knifefish (Metzen et al., 2016). These fish live in murky water and produce electric signals in order to “see” their environment. Such fish are known as weakly electric fish because the electrical discharges they produce, while strong enough to "see" objects, are not strong enough to be used as weapons.

A brown ghost knifefish emits an electric field that oscillates at a given frequency and creates an electric field that surrounds the fish. It also uses an array of electroreceptors on its surface to detect changes in this electric field: these changes could be caused by other fish, both electric and non-electric, predator or prey, as well as other objects. Metzen et al. focused on what happens when a knifefish communicates with another knifefish. Each knifefish emits at a slightly different frequency, so when two knifefish come into close proximity of each other, these frequencies interfere to generate a beat pattern. The frequency of this beat pattern is equal to the difference between the two original frequencies.

If a knifefish wants to communicate with another knifefish, it produces a “chirp” – a temporary increase in the frequency of its electric field discharge (Zupanc and Maler 1993; Figure 1). This leads to a change in both the frequency and phase of the beat pattern (with the change in the phase having any value between zero and 360 degrees). The phase can change again (by between zero and 360 degrees) depending upon the timing of the response from the second fish. Given this ambiguity, how can the fish recognize each other when each fish can produce a wide range of different phase changes in the beat pattern?

Weakly electric fish generate electric fields to communicate and to probe their environment.

(A) The electric fields produced by two electric fish (red and blue lines; top) interfere to produce a beat pattern (brown and black lines; middle); the horizontal red and blue lines indicate that the frequency of each field does not change with time. If the red fish wants to communicate with the blue fish, it increases the frequency of the electric field it produces for a short time (red-green-red line; bottom). This "chirp" changes both the frequency and phase of the beat pattern (brown and black lines; bottom). Image from Metzen et al. (B) Computer simulation (computed using the dipole approximation) showing the electric fields produced by two electric fish. The fish on the left is able to detect the presence of the fish on the right because the latter changes the electric field in the vicinity of the former, and vice versa. The different colors represent different strengths and directions of the electric field.

Metzen et al. studied how the communication signal is represented in three successive stages of neural circuits: circuits formed by neurons that are directly connected to the electroreceptors on the surface of the fish; circuits formed by pyramidal neurons in the hindbrain; and circuits formed by neurons within the Torus semicircularis in the midbrain. Metzen et al. report that neural responses at each successive stage of processing depend less and less on the phase. This process of making the signals 'phase invariant' is similar to how visual signals are processed (Movshon et al., 1978; Sharpee et al., 2013).

Studies of the comparatively simple neural circuits of the weakly electric fish can also provide insights into the neural mechanisms behind invariant responses in other more complex sensory systems. For example, the responses of the individual peripheral neurons in the knifefish are not phase invariant: however, the activity of these neurons is correlated in a way that is phase invariant. This shows that one way to generate a phase-invariant response is to correlate and combine a number of neural responses.

A prominent aspect of electrosensation is that the animal has control over the types of signals that it produces. This makes it a rich ground for testing the theory that biological circuits are optimized to transmit maximal information for a given cost (Polani, 2009; Bialek, 2013). Relevant questions include: why are the electro-receptors on the surface of the fish distributed the way they are, and why do the communication calls used by knifefish have the structure they do? And given that fish continue to grow throughout their lives, how does the electrosensory system continue to operate when the anatomy of the fish is changing constantly? An answer to this last question could help to improve our understanding of how mammalian systems cope with aging and adaptation (Webster et al., 2006).

More generally, one expects to find many solutions to the problem of information optimization, depending on the characteristics of the environmental niche for a particular animal and the metabolic costs they can afford (Tishby and Polani, 2011). The diversity of these solutions can be mapped onto biological diversity. For example, why do some fish probe their environment with electric fields, whereas bats use echolocation? From a computational perspective, there are also parallels between electrosensation in weakly electric fish and song communication in birds, auditory vocalizations in dolphins and non-human primates, and human speech (Kanwal and Rauschecker, 2007). Comparative analysis of these systems in terms of information and energy efficiency will help to elucidate the general principles of how neural circuits work.

References

  1. Book
    1. Tishby N
    2. Polani D
    (2011) Information theory of decisions and actions
    In: Cutsuridis V, Hussain A, Taylor JG, editors. Perception-Action Cycle. New York: Springer. pp. 601–636.
    https://doi.org/10.1007/978-1-4419-1452-1_19
  2. Book
    1. Bialek W
    (2013)
    Biophysics Searching for Principles
    Princeton, NJ: Princeton University Press.
    1. Sharpee TO
    2. Kouh M
    3. Reynolds JH
    (2013) Trade-off between curvature tuning and position invariance in visual area V4
    Proceedings of the National Academy of Sciences of the United States of America 110:11618–11623.
    https://doi.org/10.1073/pnas.1217479110

Article and author information

Author details

  1. Tatyana O Sharpee

    Computational Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    For correspondence
    sharpee@salk.edu
    Competing interests
    The author declares that no competing interests exist.

Publication history

  1. Version of Record published:

Copyright

© 2016, Sharpee

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 891
    views
  • 115
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Tatyana O Sharpee
(2016)
Neural Coding: Taking a close look at electrosensing
eLife 5:e16209.
https://doi.org/10.7554/eLife.16209

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Jian Qiu, Margaritis Voliotis ... Martin J Kelly
    Research Article

    Hypothalamic kisspeptin (Kiss1) neurons are vital for pubertal development and reproduction. Arcuate nucleus Kiss1 (Kiss1ARH) neurons are responsible for the pulsatile release of gonadotropin-releasing hormone (GnRH). In females, the behavior of Kiss1ARH neurons, expressing Kiss1, neurokinin B (NKB), and dynorphin (Dyn), varies throughout the ovarian cycle. Studies indicate that 17β-estradiol (E2) reduces peptide expression but increases Slc17a6 (Vglut2) mRNA and glutamate neurotransmission in these neurons, suggesting a shift from peptidergic to glutamatergic signaling. To investigate this shift, we combined transcriptomics, electrophysiology, and mathematical modeling. Our results demonstrate that E2 treatment upregulates the mRNA expression of voltage-activated calcium channels, elevating the whole-cell calcium current that contributes to high-frequency burst firing. Additionally, E2 treatment decreased the mRNA levels of canonical transient receptor potential (TPRC) 5 and G protein-coupled K+ (GIRK) channels. When Trpc5 channels in Kiss1ARH neurons were deleted using CRISPR/SaCas9, the slow excitatory postsynaptic potential was eliminated. Our data enabled us to formulate a biophysically realistic mathematical model of Kiss1ARH neurons, suggesting that E2 modifies ionic conductances in these neurons, enabling the transition from high-frequency synchronous firing through NKB-driven activation of TRPC5 channels to a short bursting mode facilitating glutamate release. In a low E2 milieu, synchronous firing of Kiss1ARH neurons drives pulsatile release of GnRH, while the transition to burst firing with high, preovulatory levels of E2 would facilitate the GnRH surge through its glutamatergic synaptic connection to preoptic Kiss1 neurons.

    1. Computational and Systems Biology
    David B Blumenthal, Marta Lucchetta ... Martin H Schaefer
    Research Article

    Degree distributions in protein-protein interaction (PPI) networks are believed to follow a power law (PL). However, technical and study bias affect the experimental procedures for detecting PPIs. For instance, cancer-associated proteins have received disproportional attention. Moreover, bait proteins in large-scale experiments tend to have many false-positive interaction partners. Studying the degree distributions of thousands of PPI networks of controlled provenance, we address the question if PL distributions in observed PPI networks could be explained by these biases alone. Our findings are supported by mathematical models and extensive simulations and indicate that study bias and technical bias suffice to produce the observed PL distribution. It is, hence, problematic to derive hypotheses about the topology of the true biological interactome from the PL distributions in observed PPI networks. Our study casts doubt on the use of the PL property of biological networks as a modeling assumption or quality criterion in network biology.