Representationalism and Olfactory Valence

A distinction that is particularly important in the context of evaluating the Indicative Hypothesis and the Satisfaction Hypothesis concerns a division between unidimensional and bidimensional coding of valence. In the case of bidimensional coding, pleasure and displeasure are encoded separately, such that a stimulus is assessed as both pleasant and unpleasant to a certain degree. In abstract terms, we can model this situation by distinguishing two scales: a positive scale that encodes pleasure, P:[0, . ., MAX], and a negative scale that encodes displeasure, N:[0, . ., MAX]. Every olfactory stimulus is assigned a value on each scale, such that a 0 on scale P means lack of pleasure, 0 on N means lack of displeasure, and MAX values designate maximal pleasure (scale P) or maximal displeasure (scale N).

Analogously, unidimensional coding can be modelled using a single scale, V:[− MAX,. . ., NEU,. . ., +MAX], encoding both pleasure and displeasure. On a unidimensional scale V, the value –MAX corresponds to maximal displeasure, +MAX corresponds to maximal pleasure, and NEU designates neutral valence. Contrary to bidimensional coding, a stimulus encoded on a unidimensional scale cannot be characterised as both pleasurable and unpleasurable, since stimuli are assigned a single value corresponding to either a certain degree of pleasure or a certain degree of displeasure.

Two brain regions that are strongly involved in encoding olfactory valence are the amygdala (Jin et al. 2015; Root et al. 2014; Sosulski et al. 2011) and the orbitofrontal cortex (Grabenhorst et al. 2007; Lundström et al. 2006; Zelao et al. 2007). While some earlier research suggested that the amygdala processes only the intensity of odours and not their valence (see Anderson et al. 2003), there is now considerable evidence that the amygdala encodes valence in a unidimensional manner. More specifically, the amygdala encodes olfactory valence in a unidimensional manner if (a) it encodes both positive and negative valence, and (b) there is a continuity of neural patterns from maximum pleasure to maximum displeasure, such that patterns for maximum pleasure and maximum displeasure are least similar, and patterns for low pleasure and low displeasure are quite similar. In contrast, when valence is encoded bidimensionally, there is no such continuity of neural patterns. In particular, patterns encoding low pleasure and low displeasure should not be similar.

The first point is widely accepted in the contemporary empirical literature (see O’Neill et al. 2018; Smith and Torregrossa 2021 for reviews). In particular, single-cell recordings (Iwaoki and Nakamura 2022; Sadacca et al. 2012) and electrophysiological studies (Beyeler et al. 2016, 2018; Kim et al. 2016; Namburi et al. 2015) on non-human mammals have allowed the identification of neuronal populations in the amygdala that encode positive and negative valence. These studies were conducted on several species, in particular rodents and monkeys, using stimuli associated with chemical, auditory and visual modalities. Such results make it very likely that in the case of the human sensory system the amygdala also encodes both positive and negative valence associated with olfactory stimuli.

The question of whether valence is encoded in the amygdala in such a way that there is continuity of neural patterns from those associated with positive valence to those associated with negative valence is more controversial. Nevertheless, the available data suggest that a unidimensional coding of valence in the amygdala should at least be treated as a serious hypothesis.

First, it has been observed that populations of neurons in the amygdala that encode positive and negative valence are anatomically partially intermixed (Beyeler et, al., 2018) and that the valence-related activities of these populations overlap (see Namburi et al. 2015 for ex vivo electrophysiological studies on mice). Furthermore, Iwaoki and Nakamura (2022), using single-cell recording studies on monkeys, have shown that the amygdala contains neurons that are activated by both a strongly pleasant and a weakly unpleasant stimulus, as well as neurons that are conversely activated by both a strongly unpleasant and a weakly pleasant stimulus. Such results suggest that the neural patterns associated with positive and negative valence are not separate, as some cells respond to both positively and negatively valenced stimuli.

Second, it has been shown that there are inhibitory relations between cell populations encoding valence in the amygdala (see Beyeler et al. 2016; Kim et al. 2016; Wang et al. 2018): activities of populations encoding positive valence inhibit activations of populations encoding negative valence and vice versa. If such inhibitory relationships are present, it is likely that neural patterns associated with strong pleasantness and strong unpleasantness will be dissimilar. A highly valenced stimulus will cause strong activation in one population and consequently strong inhibition of the population encoding the opposite valence. On the other hand, the neural patterns associated with weak pleasantness and weak unpleasantness are likely to be more similar, because whatever the valence of the stimulus, one population will be weakly activated and the other weakly inhibited.

Third, more direct evidence for the continuity of valence-encoding neural patterns, specifically in relation to olfactory stimulation and the human amygdala, was obtained in an fMRI study by Jin et al. (2015). In their experiment, people were exposed to a series of nine olfactory stimuli, ranging from very pleasant to very unpleasant. The researchers observed that as the stimulus valence changed from maximally positive to maximally negative, the patterns of neural activation also gradually changed in a way that is required by unidimensional coding. Analogous results were obtained in the fMRI study by Tiedemann et al. (2020) using visual food-related stimuli. Although the study by Tiedemann et al. (2020) did not involve olfaction, the results, together with those obtained by Jin et al. (2015), suggest that the human amygdala unidimensionally encodes valence in the context of stimuli relevant to food evaluation.

Taken together, the above results show that not only does the amygdala encode both positive and negative valence, but also that (a) opposite valences are not encoded by completely separate neural populations, (b) due to inhibitory relationships, it is likely that neural patterns associated with strong positive and negative valence are less similar to each other than those associated with weak positive and negative valence, and (c) there are fMRI studies on the human amygdala whose results suggest the continuity of neural activation patterns between those encoding strong positive valence and those encoding strong negative valence. I believe that, although we do not have complete knowledge of the encoding of olfactory valence, these results taken together show that a unidimensional encoding of valence in the amygdala is a plausible possibility.

However, these observations cannot be automatically extrapolated to all neural regions involved in encoding olfactory valence. For example, studies on the perception of olfactory stimuli with ambiguous valence suggest that olfactory valence is bidimensionally encoded in the orbitofrontal cortex. In particular, an fMRI study by Grabenhorst et al. (2007), using jasmine, indole and their combinations as stimuli, has shown that an ambiguous olfactory stimulus simultaneously activates separate regions in the medial and middle orbitofrontal cortex that encode the stimulus as both pleasant and unpleasant. This anatomical separation allows the simultaneous encoding of negative and positive valence without mutual interference.

Hence, relying on results regarding valence encoding in amygdala, I accept the following assumption:

(Unidimensional Encoding) Olfactory valence in the human olfactory system is, at least partially, encoded unidimensionally.

Later, for short, I name the neural patterns which encode information about olfactory valence “valence-codes”.

Of course, philosophical theories of sensory pleasure do not concern neural coding but contents of hedonic mental states which determine the olfactory valence. Hence, in order to formulate an argument relating these theories to ways of neural encoding one has to propose some relationship between neural codes and contents of hedonic states. In this respect, my argument requires only an intuitive assumption that (a) contents of hedonic states which determine valence are encoded by valence-codes and (b) similar valence-codes correspond to similar contents, i.e. contents which determine similar valences. For instance, indicative representational content A is a little bad for a subject should have a more similar neural code to content A is moderately bad for a subject than to content A is very bad for a subjectFootnote 1. Analogously, a positive content of a desire that a stimulation should continue will have quite different neural code to a negative content of a desire that a stimulation should stop.

From the perspective of the considered philosophical theories, the experienced olfactory valence is determined by the contents of olfactory hedonic states. On the other hand, from the neuroscientific perspective, the information which allows determining olfactory valence is encoded by certain neural patterns, which I call “valence-codes”. In addition, philosophical theories usually accept a general naturalistic assumption that contents of mental states are somehow neurally encoded. Hence, if we want to combine the philosophical and neuroscientific approach to olfactory valence, it is plausible to postulate that contents determining olfactory valence are encoded by the neural valence-codes. It should be noted hat this does not mean that the presence of certain neural codes is sufficient for conscious hedonic experiences. It is likely that, for a conscious experience, the encoded information has to be additionally represented by a higher-order state (as postulated by higher-order theories of consciousness, e.g., Rosenthal 2005) or must be available in a global workspace (e.g., Baars 2005).

Furthermore, if similar contents were not encoded by similar valence-codes, it would be unclear in virtue of what certain valence-codes correspond to certain contents as there would be no systematic relationship between the characteristics of valence-codes and the characteristics of contents which determine olfactory valences. In consequence, I accept the following Similarity assumption:

(Similarity) Contents of hedonic olfactory experiences which determine the olfactory valence are neurally encoded by valence-codes such that similar contents, i.e. determining similar valences, are encoded by similar valence-codes.

Nevertheless, an additional complication arises due to the fact that plausibly there is more than one type of valence-codes, and, on the other hand, there may be more than one type of content determining the olfactory valence. First, as shown earlier, it is likely that olfactory valence is encoded in several distinct places, like the amygdala and the orbitofrontal cortex, possibly by using different types of coding (unidimensional and bidimensional). Second, it is often proposed that a single hedonic experience may be associated with several contents that determine distinct aspects of pleasantness or unpleasantness (see Coninx and Stilwell, 2021; Cutter and Tye 2014; Boswell 2016).

In consequence, a question arises as to how to match the distinct types of valence-codes with distinct types of contents determining various aspects of olfactory valence. Four major answers are possible. First, it may be claimed that there is no matching: types of valence-codes are not associated with types of contents determining valence. However, as argued earlier, such an option is unlikely at it is plausible to assume that contents determining valence are encoded by valence-codes.

Second, one may propose that some types of valence-codes encode contents of olfactory hedonic states, but other types of valence-codes do not encode any such contents. For instance, maybe unidimensional valence-codes in the amygdala does not encode any contents of hedonic states, but bidimensional valence-codes in the orbitofrontal cortex encode such contents. However, this option is also unlikely as it seems ad hoc to postulate that only some types of valence-codes correspond to contents of hedonic states if all these types of neural patterns are such that they encode information about the olfactory valence.

Third, it may be the case that distinct types of valence-codes are associated with distinct types of contents, i.e. which determine distinct aspects of valence. For instance, one may propose that unidimensional valence-codes in the amygdala encode contents determining the basic sensory unpleasantness caused by properties of the stimulus, while bidimensional valence-codes in the orbitofrontal cortex encode contents that determine the sensory unpleasantness modified by top-down factors. I believe it is a plausible option without obvious reasons to be rejected.

Finally, it is possible that some type of content determining a single aspect of olfactory valence is encoded jointly by more than one type of valence-code. For instance, an aspect of the olfactory valence may be determined by a content composed of two parts, one encoded unidimensionally and the second encoded bidimensionally. As with the previous option, there are no strong reasons why this could not be the case.

My argumentation does not require formulating a complete answer to the issue of matching between types of valence-codes and types of content determining olfactory valence. It only requires an assumption that the third or fourth of the above options, i.e. one of the two most plausible options, is true. If one of these options is true, and Unidimensional Encoding and Similarity assumptions are endorsed, then there is at least one type of content of hedonic states which determine an aspect of olfactory valence such that at least part of this content is encoded unidimensionally. The Unidimensional Encoding and Similarity jointly entail that there are unidimensional valence-codes and contents determining valence are encoded by valence-codes. If, as argued above, it is not likely that there are valence-codes which do not encode any part of content determining valence, then some content determining valence is, at least partially, encoded unidimensionally.

This postulate is expressed in the following Matching assumption:

(Matching) There is a type of hedonic states’ content which determines an aspect of olfactory valence, such that at least part of this content is unidimensionally encoded.

The above three assumptions constitute background on which my argument is presented. First, according to the Unidimensional Encoding assumption the olfactory valence is, at least partially, encoded unidimensionally. This assumption seems reasonable given the neuroscientific studies on olfaction. Second, the Similarity assumptions states that contents of hedonic states which determine olfactory valence are encoded by valence-codes such that similar valence-codes encode similar contents. I have argued that such a postulate is plausible if one wants to combine philosophical theories of sensory pleasure with the way in which valence is neurally encoded. Finally, according to the Matching assumption, there is a type of hedonic state content which determines an aspect of olfactory valence such that at least part of this content is unidimensionally encoded. This assumption is consistent with the most plausible ideas regarding the connection between types of valence-codes and types of contents determining olfactory valence.

Based on these three assumptions, Unidimensional Encoding, Similarity and Matching, I can present further steps of my argument. First, I show that unidimensional coding is incompatible with the categorical content assumed in satisfaction theories. Second, I argue that the analogous problem is not present in the case of indicatively representational theories because they adopt quantitative content. Finally, I show that satisfaction theories cannot easily adopt quantitative content. Consequently, it is unlikely that satisfaction theories can fully account for olfactory valence.

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