It's all about deforming the phenotype. COURTESY: DiPaola, Evolving Darwin's Gaze (click to enlarge).
For this year's Darwin Day (February 12), I will be discussing a classic Neuroscience experiment by Roger Sperry [1]. This was discussed recently on Twitter (Figures 1 and 3), along with a movie (Movie 1) that demonstrates the behavioral effect of this manipulation. In the movie, we can see before and after behaviors with respect to prey capture. Before the manipulation, the frog seamlessly captures flies with a flick of the tongue. Afterward, the frog flicks in precisely the opposite direction of the fly. What is the biology behind this manipulation, and why does the manipulation produce seemingly maladaptive behavior?
Figure 1. Tweet on Sperry's eye rotation experiment and chemosensory hypothesis (click to enlarge).
Movie 1. Video demonstration of Sperry's eye rotation experiment (click to enlarge).
In conducting this experiment, a frog's eyes are surgically rotated 180 degrees about each socket (see Figure 2). Due to this treatment, the normal course of axonogenesis between the eyeball and the tectum (part of the frog brain) is distorted [2]. As a result, the connections are shifted and the visual information is mapped to different regions of the tectum. The tectum serves as a visuospatial map of the environment, and maps visual stimuli to a reference frame used to generate motor behavior. As the reference frame is than systematically rotates, so is the frog's movement behavior. Thus, our manipulated frog produces a tongue flick that is 180 degrees in the opposite direction of the prey it is trying to capture.
Figure 2. Cartoon demonstrating chemosensory hypothesis and behavioral effects of eye rotation experiment (click to enlarge).
What is known as the chemosensory hypothesis (see Figure 2) also provided support for another concept, that of experience-dependent plasticity. The second tweet (below) discusses how this concept explains (and does not explain) what we see in the frog tectum and its modified behavior.
Figure 3. Part of response to tweet in Figure 1, with an assessment of the functional consequences (click to enlarge).
Roger Sperry is also known for another set of experiments conducted a few years later [3] that asked whether neuroplasticity was a real phenomenon (as opposed to an epiphenomenon). This was done by either abnormally innervating muscle or placing end-effectors (limbs) in maladaptive locations on the body. If the organism could overcome these changes, such changes could be overcome via adaptation. As in the case of the eye rotation experiment, motor patterns are not plastic, even when neuronal connections are non-specific. This is why the eye rotated frog cannot adjust its behavior to adaptation in the spatial representation of visual input.
Figure 4. A demonstration of conduction delay in the quadruped hindlimb in relation to multiple components of the sensorimotor loop. COURTESY: Figure 1 in [7] (click to enlarge).
So what does this have to do with evolution by natural selection [4]? It turns out that there are scaling laws that govern the coordination of the nervous system and phenotype as they both emerge in development [5]. Specifically, there are characteristically proportional relationships between motor neuron innervation and target tissue size in different parts of the organism [5, Note 1]. This developmental relationship (which holds true across related species) leads to interesting functional consequences. More et.al [6] suggests a trade-off in sensorimotor systems between responsiveness (temporal respond to stimuli) and resolution (sensory discrimination translated into muscle force production) results from size variation across phylogeny.
Figure 5. Scaling of various sources of delay across species. Scaling comparison is in terms of mass (kg) versus delay (ms). COURTESY: Figure 2 in [7] (click to enlarge).
This relationship between size and a responsiveness-resolution trade-off also affects behavior. More and Donelan [7] show that conduction delay (an indicator of reaction time) also scales with variation in organismal size (Figure 4). The delay in force production (behavioral output) can be explained mostly in terms of nerve conduction delay rather than a delay in the sensory or synaptic components of the sensorimotor loop (Figure 5). This suggests a fundamental constraint on motor behavior that is independent of sensory inputs or their neural representation. But notice what is said about frog tectum in Figure 3: while eye saccades and tongue movement that produce the movement itself are not controlled by the tectum, a triggering threshold results from the active representation of visual information.
Through the efficiency of population coding [8], this representation determines the timing of movement execution, which occurs in spatial context along with an appropriate amount of force. Perhaps the rotated eye manipulation (and associated phenomena like the prism experiment) presents an interesting exception to the responsiveness/resolution trade-off. Perhaps an intervening variable, representational alignment, also affects the linearity of the primary trade-off for specific movement behaviors. Across different species with common ancestry [9], this could become quite variable, and even provide an evolutionary-based account of neural plasticity.
NOTES:
[1] Sperry, R.W. (1943). Effect of 180 Degree Rotation of the Retinal Field on Visuomotor Coordination. Journal of Experimental Zoology, 92(3), 263–279.
[2] the reference to chemoaffinity in the first tweet refers to the process of axons finding their way to a target tissue. This is the basis for Sperry's "chemoaffinity hypothesis". Please see: Meyer, R.L. (1998). Roger Sperry and his chemoaffinity hypothesis. Neuropsychologia, 36 (10), 957–980.
[3] Sperry, R.W. (1945). The Problem of Central Nervous Reorganization After Nerve Regeneration and Muscle Transposition. Quarterly Review of Biology, 20(4), 311-369.
[4] For more on this topic, please see the following Synthetic Daisies posts:
The Evolution and Neuromechanics of very-fast movements. January 24, 2012
The Neuromechanics and Evolution of Very Slow Movements. April 18, 2012
Perceptual Time and the Evolution of Informational Investment. September 24, 2013
[5] Striedter, G.F. (2004). Principles of Brain Evolution. Oxford University Press, Oxford, UK.
[6] More, H.L., Hutchinson, J.R., Collins, D.F., Weber, D.J., Aung, S.K.H., and Donelan, J.M. (2010). Scaling of sensorimotor control in terrestrial mammals. Royal Society of London B, 277(1700), 3563-3568.
[7] More, H.L. and Donelan, J.M. (2018). Scaling of sensorimotor delays in terrestrial mammals. Royal Society of London B, 285(1855), 20180613.
[8] Shamir, M. (2014). Emerging principles of population coding: in search for the neural code. Current Opinion in Neurobiology, 25, 140-148 AND Pouget, A., Dayan, P., & Zemel, R. (2000). Information processing with population codes. Nature Reviews Neuroscience, 1, 125–132.
[9] Quian Quiroga, R. (2019). Neural representations across species. Science, 363(6434), 1388-1389.
