Smell, fear and sensory learning

Blogging on Peer-Reviewed ResearchWen Li, James D. Howard, Todd B. Parrish, and Jay A. Gottfried have a fascinating article in the most recent edition of Science, ‘Aversive Learning Enhances Perceptual and Cortical Discrimination of Indiscriminable Odor Cues.’ The researchers trained subjects to discern between the aroma of chemicals that initially were indistinguishable using electric shocks (!) coupled with one of the two aromas. The research is a great example of perceptual learning, a form of neural enculturation that I think is absolutely essential to understanding cultural difference but little appreciated in anthropology.

Subjects in the experiment were given a test of their ability to discern between very closely related chemicals: ‘On each trial, subjects smelled sets of three bottles (two containing one odorant, the third containing its chiral opposite) and selected the odd stimulus.’ Before the training, subjects selected the odd odor out 33% of the time — no better than random. After the repeated association of one chemical with shocks, subjects’ ability to discriminate the smells improved markedly, showing that negative reinforcement training could ‘enhance perceptual discriminability between initially indistinguishable odors.’ Moreover, the neural representation of the smells changed, as found with fMRI.

From their abstract:

We combined multivariate functional magnetic resonance imaging with olfactory psychophysics to show that initially indistinguishable odor enantiomers (mirror-image molecules) become discriminable after aversive conditioning, paralleling the spatial divergence of ensemble activity patterns in primary olfactory (piriform) cortex. Our findings indicate that aversive learning induces piriform plasticity with corresponding gains in odor enantiomer discrimination, underscoring the capacity of fear conditioning to update perceptual representation of predictive cues, over and above its well-recognized role in the acquisition of conditioned responses. That completely indiscriminable sensations can be transformed into discriminable percepts further accentuates the potency of associative learning to enhance sensory cue perception and support adaptive behavior.

The focus of part of the research, and of some of the comments at the blog, Ars Technica (see below), is on the negative conditioning, in part because of the researchers assumptions about the ‘evolutionary significance’ of the ability to sense. The authors suggest, in the opening to the article: ‘The ability to minimize contact with aversive experience is a hallmark of adaptive behavior. Via mechanisms of associative learning, organisms can use sensory information in the environment to predict impending danger and initiate fight-or-flight responses.’ The authors go on with a kind of evolutionary story about needing to discern the difference in smell between a 175-kg lion and a 3-kg house cat, an odd evolutionary story considering how long cats have been domesticated.

While I agree with this statement, and find the research fascinating, I don’t want to oversell the ‘negative conditioning’ dimension or assume that this is the only emotional mechanism the might be linked to perceptual learning. That is, some sensory plasticity seems also to be driven by reward or positive conditioning, but we’ll miss this if we have an overly simplistic assumption about perceptual learning always being driven by negative, survival threats. For example, one of the comments at Ars Technica jokes about the need for corporal punishment in schools; I know the poster is kidding, but I think there is the danger of over-emphasizing the need for negative reinforcement. And there’s a danger of overly simplistic accounts of how evolution might have acted on our senses.

In fact, the researchers conclude that the learning mechanism involved is not dependent upon the fear caused by the electrical stimuli: ‘The results further show that fear conditioning to an odor cue recruits many of the same regions involved in conditioning to visual and auditory cues, emphasizing the multimodal versatility of these learning networks.’ Although this particular experiment may have recruited parts of the brain associated with fear (the amygdala and orbito-frontal cortex) into a neural system able to discern these fear-inspiring scents, the fear-related ‘nodes’ of this neural network may not have been necessary for the perceptual refinement to occur. No doubt, fear was an efficient way to cause this system to change, but other neural resources might have been capable of reconfiguring the system as well.

Other evidence of sensory plasticity suggest that strongly motivated people can be trained for heightened olfactory sensitivity without strong fear or pain being involved. The most obvious example with olfaction is the training of perfume testers and wine tasters. Both fields used kits with distilled scent samples in order to train up the sense of smell until people can become quite sophisticated and discerning. Similar evidence can be found of sensory plasticity in vision, hearing, and other senses depending upon training; the point for me is that the sense is plastic, not that we always need to suffer or fear in order to develop more acute senses. (I won’t use examples from sports—like I always do—but there are plenty.) The issue for me is an overly simplistic explanation of human neural plasticity; that we ‘adapt’ to things we need to fear. Yes, but our nervous systems also sharpen, shift, and reallocate resources for other reasons to, most often just because we are motivated and use the sense, demanding of it greater skill.

In addition to my slight issue with the notion that fear needs to be involved (and in several places in the article, it seems to me that the authors are saying the same thing), I think that there’s a more important take away from this article for anthropologists. In general, the anthropological study of the senses has not addressed the possibility that the senses themselves might be shaped by cultural patterns of training, experience, and behavior. Anthropologists have tended to argue that senses can mean something different to various groups, or that sensory information might be interpreted differently, but they haven’t really considered the likelihood that different groups are just not experiencing the same things.

Many of these differences wouldn’t be because of some inevitable, pre-ordained, innate variation in the way that our senses work (although I won’t rule that possibility out). Rather, like the ability to discern between ‘tgCS+’ and its related scent, ‘chCS+,’ the two chemicals used in this experiment by Li and colleagues, most differences will be acquired, resulting from perceptual plasticity or perceptual learning. The reason I suggest this is not just because of some ideological commitment to ‘nurture’ influences, but because the sensory systems of humans enter this world needing quite a bit of input to become fully functional.

This kind of sensory learning, a shifting and refinement of the nervous system due to experience and training, is one reason that I’ve pushed to call what Daniel and I and others are now doing ‘neuroanthropology’ rather than ‘cognitive anthropology,’ although I take quite a bit from those scholars who label themselves ‘cognitive anthropologists.’ Just as the over-emphasis on fear and ‘adaptation’ as frames for understanding changes in the brain, such as the one in the subjects of this experiment, framing it as a ‘cognitive’ change also has the potential to distort the significance of these findings. And so I’ll just end with what I think is the bottom line.

Li and colleagues were able to train people to be able to smell a distinction that they couldn’t smell before, and there was a shifting of the physical parts of the brain involved in detecting these chemicals once this ability was acquired. Although fear was the motivation here, it is possible that this is not absolutely necessary, and we can’t tell from the research wether or not ‘consciousness’ was directly involved or necessary to the process (although subjects were certainly aware that they were shocked, they might not be able to consciously discriminate between the scents).

Acknowledgment: Thanks to John Timmer at Ars Technica for his posting, Improving human olfaction through pain, which led me to the original article in Science.

Wen Li, James D. Howard, Todd B. Parrish, and Jay A. Gottfried. 2008. Aversive Learning Enhances Perceptual and Cortical Discrimination of Indiscriminable Odor Cues. Science 319 (5871): 1842-1845. doi: 10.1126/science.1152837 (abstract here)

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Trained as a cultural anthropologist at the University of Chicago, I have gone on to do fieldwork in Brazil and the United States. I have written one book, Learning Capoeira: Lessons in Cunning from an Afro-Brazilian Art (Oxford, 2005). I have also co-authored and co-edited several, including, with Dr. Daniel Lende, The Encultured Brain: An Introduction to Neuroanthropology (MIT, 2012), and with Dr. Melissa Fisher, Frontiers of Capital: Ethnographic Reflections on the New Economy (Duke, 2006). My research interests include neuroanthropology, psychological anthropology, sport, dance, human rights, neuroscience, phenomenology, economic anthropology, and just about anything else that catches my attention.

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