Wiederorientierung in Bats and the Nature of Animal Consciousness

1. Wiederorientierung in Bats and the Nature of Animal Consciousness Harry R. Erwin, PhD University of Sunderland School of Computing and Technology

2. Or “Why does the bat do it?” • Experimental results from behavioural and computational research performed with Cynthia F. Moss, Ph.D., at the the Auditory Neuro-ethology Laboratory, Department of Psychology, University of Maryland, College Park. • With thanks to Willard Wilson, Peter Abrams, Myriam Tron, Amy Kryjak, and Paul Kelley. • Further research at the School of Computing and Technology, University of Sunderland.

3. Nagel’s thesis (Nagel, T., What is it like to be a bat? The Philosophical Review, 1974. 83(4): p. 435-450.) • Nagel criticized reductionist and materialist approaches to the mind-body problem, taking the position that consciousness made the problem intractable. He pointed at bat biosonar as a sense we could not understand, so preventing us from truly understanding the conscious life of bats. • He ended with a proposal for an objective phenomenology independent of imagination or empathy, so questions on the physical basis of existence could become intelligible.

4. What is it to be a bat? • Nagel used echolocating bats as examples of organisms with alien experience. He stated, “bat sonar, …, is not similar in its operation to any sense that we possess, and there is no reason to suppose that it is subjectively like anything we can experience or imagine….” • He then suggested we cannot extrapolate to the inner life of a bat from our own experience, putting the subjective experience of the bat beyond the reach of objective science. • So where is his argument today?

5. Our basic research question: how bats capture prey using biosonar • Figure from Webster and Brazier, Experimental Studies on Target Detection, Evaluation and Interception by Echo-locating Bats , 1965 • A bat (Myotis lucifugus) capturing a moth in foliage. • 100 millisecond intervals • The bat had first detected the tree about 500 milliseconds before the first image. • Data available to the bat—a few biosonar snapshots in the dark.

6. Early hints: Erstorientierung and Wiederorientierung • Reported by Möhres and Öttingen-Spielberg in 1949. Erstorientierung—when bats first encounter a novel situation. Wiederorientierung—when bats fly in a familiar space. • First observed in the behaviour of a bat that was accustomed to roosting in a cage in a room. The researchers rotated the cage and eventually removed it, and noted that the bat continued to behave as if the cage were in its normal position until forced to reorient. • This was evidence that a bat uses and maintains a world model that is only modified if circumstances force it to. The bat lives in this world model and uses it to choose its behaviour—intentionally. • This has also been seen in rodent behaviour.

7. Experimental evidence • Biosonar is a basic mammalian capability. Most mammals can use passive techniques, and some are even capable of active echolocation. At the same time, ‘whispering’ bats have been identified that use passive biosonar to hunt insects. • In humans, auditory localization is termed ‘active vision’, and involves the use of both passive and active biosonar. • The brain structures underlying these processes in the bat are quantitatively, not qualitatively, different from those in our brain.

8. Mechanisms of biosonar • We now understand better how biosonar works in most mammals. • Azimuth is estimated from both relative time delays and sound shadowing by the head and pinnae. • Elevation is estimated from spectral phenomena and by rotating the horizontal axis. • Range is estimated from echo-delay time and triangulation. • Other mechanisms may play a role, but these are the primary ones, even in bats.

9. Bat sonar and ‘facial vision’ • Humans localize sounds well. • Human ‘facial vision’ is primarily passive biosonar with 3-D localization of objects done using triangulation. The subject has to be able to move to get accurate results. • Humans can also use active biosonar (based on detecting echoes from clicks or other sounds) to map out a volume. • Both are effortful, but can be done in real-time. (Ref: discussions with Dr. Lawrence Scadden (about 1998); Griffin, D. R. (1958). Listening in the Dark. Ithaca, New York, Comstock Publishing Associates; White, J. C., Saunders, F. A., Scadden, L., Bach-y-Rita, P., & Collins, C. C. (1970). Seeing with the skin. Perception & Psychophysics,7, 23-27.)

10. So it is possible to understand how the bat perceives the world • Biosonar is effortful and restricted to low frequency in humans (50-25000 Hz). It is a ‘tactile’, not a ‘visual’ sense. • Wiederorienterung is particularly interesting in this context—echolocating bats do not localize objects whose position is already known to them, which suggests that they also find it effortful. • Implication: we can understand bats based on our own experience, and Nagel’s criticism loses much of its power.

11. But Nagel is right, too • Reductionism is incapable—in practice—of explaining biology, let alone consciousness. • Calculating the shape of a medium-sized protein requires more than the computational resources of the universe since the Big Bang (Davies). • A single neuron requires modelling many proteins. • To model a single brain requires modelling the simultaneous activity of billions of neurons. • Knowledge arguments assume effectively infinite computational resources.

12. Normal variation in human perception From a research project by Brian Hargreaves at Stanford University, 1999.

13. What do we know about human colour perception? • Uses cone cells containing visual proteins. • Up to four light frequencies are sampled: • Red • Green1 • Green2 • Blue • Acuity of colour perception varies independently for each frequency. • Only a small percentage of the population sees the world exactly as you do.

14. So how can we possibly understand each other? • There are recent results in neuroscience that suggest people are preadapted to communicate. • Neural circuits appear to play a role in communication that is robust to the normal variation in perception. • One of these results is the discovery of mirror neurons (Rizzolatti and Arbib).

15. The role of mirror neurons • Mirror neurons—cortical neurons that spike when a primate performs an action leading to a reward, but also when it observes another primate taking that action or when it is cued to do that action. • Found in monkey in Area F5, the premotor area, and recently in the insula. • The mirror neurons of the insula fire actively when a monkey experiences emotional sensations and also when it observes the same emotions.

16. Mirror neurons and communication • Area F5 is important in humans, because it is Broca’s area, which plays a role in human speech and communication. • The cortical areas mirror neurons are found in signal a second region of the mammalian brain, the basal ganglia, and those two regions have been observed to co-activate.

17. The basal ganglia and reward learning • The basal ganglia seem to form an ‘actor-critic’ system for the control of behaviour (Schultz). The required ‘difference signal’ has been observed. • This is proposed as a mechanism for learning the rewards associated with possible actions and simultaneously the reward value of situations (Houk, Adams & Barto). • An actor-critic model consists of two elements: • a set of ‘actors’ that learn to select actions in response to a situation using a current value function, and • a ‘critic’ that learns the current value function of the situation based on future rewards.

18. Mirror neurons and the basal ganglia • Mirror neurons may be the inputs to the basal ganglia that report the observation of rewarding actions, whether performed by the self or by others. • It is not clear whether mirror neurons are innate, but the neural circuits they use are. • Starting from innate rewards, actor-critic dynamics can support the development of a value system to guide behaviour towards rewards.

19. The development of communication • Infants learn action/state combinations leading to a reward, and these neural circuits allow them to recognize similar opportunities for others. • This produces early forms of interaction such as shared gaze, where the infant is cued to look at an object by the parent’s direction of gaze. • More complex communication can then develop from actor-independent reward perception. • The brain is preadapted to understand ‘alien’ minds by innate wiring to perceive the rewards and motivations of others.

20. What communication is • Communication is based an ‘understanding’ of the reward system of the other mind using neural circuits including mirror neurons and the basal ganglia. • Communication is a robust skill, as low-level rewards are generally similar for most mammals. • So we can realistically learn to understand ‘alien’ minds of other species (and vice versa).

21. Conclusions • Communication involves learning to ‘understand’ a reward system based on neural circuits broadly distributed among mammals. • When rewards are similar or knowable, inter-species communication is robust. • Hence, we can learn to understand ‘alien’ minds. • But that understanding cannot be based on low-level reductionist analysis. It must be high-level. • So bat experience is not fundamentally alien to us—and an objective theory of mind is possible.