Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Taste and Related Systems in Primates Including Humans
Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, UK
Correspondence to be sent to: Edmund T. Rolls, e-mail: Edmund.rolls{at}psy.ox.ac.uk
Key words: olfaction, oral temperature, oral texture, orbitofrontal cortex, primary taste cortex, taste
The cortical processing of taste and related sensory inputs is being investigated
at the neuronal level in macaques to help understand the operation of these cortical
areas in humans. The primary taste cortex of macaques in the rostral insula and adjoining
frontal operculum contains neurons tuned to different tastes including umami (Scott et al., 1986
;
Yaxley et al., 1990;
Baylis and Rolls, 1991;
Rolls et al.,
1996b, 1998). Neurons in the macaque primary taste cortex respond to
the identity and intensity of taste, in that their responses are not affected when taste
reward is decreased to zero by feeding to satiety (Rolls et al., 1988). Other neurons in the primary
taste cortex respond to somatosensory inputs by representing the viscosity of what is in
the mouth, oral fat texture, the temperature of what is in the mouth, capsaicin
(Verhagen et al., 2004), and
tannic acid (astringency) (Critchley and Rolls,
1996a). Not only are these qualities represented independently by different
neurons, but other neurons respond to combinations of these inputs (Verhagen et al., 2004). The macaque primary taste
cortex does not represent the smell or sight of food (Verhagen et al., 2004).
The macaque orbitofrontal cortex contains the secondary taste and olfactory cortices,
in that different parts of it receive from the primary taste cortex (Baylis et al., 1995), and the primary
olfactory cortical areas. Neurons in the secondary taste cortex not only represent taste,
but other neurons respond to somatosensory inputs by representing the viscosity of what
is in the mouth (Rolls et al.,
2003b), oral fat texture (Rolls
et al., 1999;
Verhagen et al., 2003), the
temperature of what is in the mouth (Kadohisa
et al., 2004), capsaicin (Kadohisa et al., 2004) and tannic acid
(astringency) (Critchley and Rolls,
1996a). Other neurons respond to combinations of these inputs. The
orbitofrontal cortex also contains neurons that respond to olfactory stimuli and to the
sight of food, and for many neurons these olfactory and taste representations are learned
by olfactory to taste or visual to taste associative learning (Rolls and Baylis, 1994;
Rolls et al., 1996a;
Critchley and Rolls, 1996b).
Orbitofrontal cortex neurons represent the reward value of what is in the mouth, in that
the neuronal responses to the taste, smell, and sight of food decrease to zero as the
monkey is fed to satiety (Rolls et al.,
1989;
Critchley and Rolls, 1996c). Further,
orbitofrontal cortex neurons represent sensory-specific reductions in their responses to
the particular foods that have been eaten to satiety, and thus implement sensory-specific
satiety (Rolls et al., 1999;
Critchley and Rolls, 1996c;
Rolls, 1999, 2004).
In human functional neuroimaging studies, it has been shown that activation of the
orbitofrontal cortex (OFC) and adjoining anterior cingulate cortex (ACC) by odours
(O'Doherty et al.,
2000) and by liquid food (Kringelbach
et al., 2003) is hunger-dependent, and indeed the pleasantness of
the food is correlated with the degree of activation found. In both studies, it was shown
that the modulation is sensory-specific, so that sensory-specific satiety is implemented
in the human OFC. The viscosity of food is represented in the human taste and non-taste
insula, and in the orbitofrontal cortex (De Araujo
and Rolls, 2004). Fat in the mouth is detected by its texture, and this is
represented in the anterior cingulate and orbitofrontal cortex (De Araujo and Rolls, 2004). The pleasantness of odours is
represented in the orbitofrontal cortex (Rolls
et al., 2003a), and flavour representations are formed by combining
taste and olfactory inputs in the orbitofrontal cortex (De Araujo et al., 2003b).
This primate neurophysiological and human functional neuroimaging evidence thus shows
that the orbitofrontal cortex is involved in decoding some primary reinforcers such as
taste, odour, texture, touch and temperature; in learning and reversing associations of
visual and other stimuli to these primary reinforcers; and in representing the
pleasantness of food in a way that correlates directly with whether food is eaten. The
orbitofrontal cortex and connected areas play key roles in representing the sensory
qualities and affective value of food, and thus in the control of eating (Rolls et al., 1990;
Rolls, 1997, 1999, 2000, 2001a,b,
2005;
O'Doherty et al.,
2001;
Rolls and Scott, 2003;
Kringelbach and Rolls, 2004).
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