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This article was originally published as a chapter in the book “Design and Catastrophe: 51 Scientists Explore Evidence in Nature"
If you have ever visited the countryside and taken a walk on a summer evening, you have most likely heard the sounds of crickets singing. These loud songs are acoustic pulses produced at specific frequencies and intensities that are meaningful and crucial for the reproduction and survival of these creatures.
Sound recognition in field crickets is rather complex and requires multiple steps that include cellular and molecular mechanisms. For instance, it requires activation of sensory receptors that tune to specific frequencies and intensities and activate higher-order neurons that provide excitatory or inhibitory input to other neurons in the prothoracic ganglion and brain of the animal. It also requires the release of specific neurotransmitters that relay action potentials across chemical synapses in nerve cells and specific receptor proteins, which are highly specific for such neurotransmitters. Ultimately, the decision of how the animal responds to the auditory signal is made in the brain, based on the information provided by auditory neurons and other local interneurons.[1]
Crickets have auditory receptors that can detect a wide range of sound frequencies. Their response to a particular auditory stimulus is indicated by whether or not they exhibit phonotaxis (i.e., the ability to move in relation to a source of sound). When female crickets are exposed to high frequency sounds, they walk away from the sound source. For these females, a high frequency sound represents a potential predator and so they exhibit negative phonotaxis.
However, in response to a lower frequency call (i.e., 4–5 kHz) the same animal will walk toward the sound source, exhibiting positive phonotaxis.[2]
How does the animal know to respond with positive phonotaxis to a given call? Several auditory neurons have been characterized in the cricket’s brain and prothoracic ganglion, which are suspected to control phonotaxis.[3] For instance, the ascending neuron 2 (AN2; or L3 in the species Acheta domesticus), which is located in the prothoracic ganglion and projects axons to the brain, is very sensitive to both 16 and 5 kHz calls.
Calls are repetitions of chirps, with each chirp containing three to four pulses of sound, called syllables. Electrophysiological recordings show that in response to 16 kHz calls, the L3 neuron produces a burst of action potentials to every single syllable of the chirp. Similar recordings show that when exposed to 5 kHz calls, the L3 not only responds with fewer action potentials overall to the lower frequency stimulus, but it also shows a decrease in the number of action potentials produced to consecutive syllables of the chirp in response to attractive calls. By manipulating the syllable period within a chirp, the calls can be made less attractive, which results in an unexpected increase in the number of L3’s action potentials. Based on this evidence, timing seems to be of utmost importance to the attractiveness of the call.[4]
The L3 neuron is just one element of a network of neurons responsible for identifying attractive calls. The fact that L3 exhibits different response patterns to 5 kHz versus 16 kHz signals indicates that various elements of the network that connect with L3 are being recruited in the response to the acoustic stimulus.[5] Such elements are providing unique information to L3, which seems to combine it and send its output to the brain for further processing. The correlation between the response of the L3 neuron to acoustic stimuli and the movement observed in the individual under study allows us to continue to investigate the underlying neural mechanisms that control phonotactic behavior in crickets.
However, a brief and partial description of how a single auditory neuron in a female cricket both responds to different stimuli and parallels phonotaxis is far from being the complete story. Additional factors such as the age of the animal, neuromodulators, hormones, and environmental temperature can further influence the neuronal and behavioral response of the animal, as can many other neurons that are involved in recognition and control of phonotaxis in the nervous system of these creatures. All of this contributes to the complexity of a recognition system that was once thought to be fixed and simple but has since been demonstrated to exhibit considerable variability as we continue to learn more about how networks of neurons control behavior. Moreover, if we think of acoustic communication between sender and receiver as a story, then reception of the signal and processing by the receiver constitute just one chapter. Additional separate chapters include production of the signal and the properties of the medium through which the sound signal travels.
It certainly requires a mastermind to design such a complex system with elements that exhibit precise tuning while allowing for variability and plasticity of the system. The alternative view is that random, undirected processes equipped an organism with key molecular elements (not discussed in this essay) required for proper functioning. Chance also provided individual neurons with intrinsic properties, such as the ability to tune to specific frequencies and integrate multiple inputs, and organized networks of neurons in ways that would allow the organism to recognize attractive from unattractive calls leading to a specific behavior. The more we learn about the details of this recognition system, the greater the conviction that randomness cannot produce such complexity and organization of life, and this only makes sense in light of an intelligent Designer.
NOTES
[1] K Schildberger. Temporal selectivity of identified auditory neurons in the cricket brain. Journal of Comparative Physiology A 1984; 155:171–185.
[2] J Stout, N Carlson, H Bingol, J Ramseier, M Bronsert, G Atkins. The L3 neuron and an associated prothoracic network are involved in calling song recognition by female crickets. Invertebrate Neuroscience 1997; 3:145–153.
[3] L Samuel, A Stumpner, G Atkins, J Stout. Processing of model calling songs by the prothoracic AN2 neurone and phonotaxis are significantly correlated in individual female Gryllus bimaculatus.
[4] Physiological Entomology 2013; 38(4):344–354. doi:10.1111/ phen.12040.for sound pattern recognition. Science Advances 2015; 1(8):e1500325.
[5] B Navia, J Stout. Prothoracic processing of models of male calling songs by female crickets: roles in behavior? Hokkaido Neuroethology Workshops, Sapporo (Japan): University of Hokkaido; 2014.
Benjamin Navia is a professor of biology at Andrews University. He earned a PhD in Biology with an emphasis in neurobiology at Loma Linda University. Along with being interested in studying the interface of faith and science, Dr. Navia is also active in investigating the neural basis of auditory behavior in invertebrat