Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
The Many Flavors of Temporal Coding in Gustatory Cortex
Psychology and Neuroscience, Volen National Center for Complex Systems/MS 013, Brandeis University, 415 South St, Waltham, MA 02454, USA
Correspondence to be sent to: Donald Katz, e-mail: dbkatz{at}brandeis.edu
Key words: behavior, cross-correlation, dynamics, electrophysiology, multiple electrodes, oscillations, synchrony
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Why temporal coding? |
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 Top Why temporal coding? ‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
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Environmental stimuli are temporally extensive. They typically (at the very least) wax and wane, and their time-varying aspects are further shaped by the behavioral responses they engender, as animals engage in approach or avoidance. Thus, neural activity related to sensation must be intrinsically time varying as well. Even if sensory stimuli were somehow punctate and static, however, neural activity would still be dynamic, because it is the job of neural brain systems to transform responses to those stimuli into activity appropriate for driving behavior, which itself unfolds as a function of time.
These statements, true in general, are particularly true of the gustatory system,
where the coupling between perception and action is virtually unbreakable: it is
impossible for an awake animal to passively observe a taste stimulus (Grill and Norgren, 1978a
;
Travers and Norgren, 1986). This
fact, and the purely neural evidence of functional feedback and convergence in forebrain
and brainstem taste relays (Smith and Li,
2000;
Lundy and Norgren, 2004), should lead
researchers to expect some sort of temporal coding in gustatory activity.
But to say that gustation involves temporal coding is to say little, because the term
‘temporal coding’ means many things to many researchers. To some the phrase
connotes ‘fast’ dynamics: the synchronous firing of neurons (e.g.
deCharms and Merzenich, 1996;
Hatsopoulos et al., 1998;
Christensen et al., 2000;
Steinmetz et al., 2000) or
neural oscillations in the ~10, ~20, or ~40 Hz range (e.g.
Eckhorn, 1994;
MacLeod et al., 1998). To
others, it refers to ‘slower’ rate changes, either in single neurons or among
coherent groups of neurons (Seidemann et
al., 1996;
Friedrich and Laurent, 2004). What
shall we say about temporal coding in the gustatory system?
Several labs including mine are currently seeking answers to this question. Thus far, the data tell the story of temporal coding being apparent mostly (but not solely) at the level of coherent rate changes among neural ensembles, perhaps driving the system toward (or reflecting) response specification. Gustatory cortical (GC) involvement in this process may extend to preparatory coding that develops across trials in learning situations.
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‘Fast’ temporal codes—oscillations and synchrony |
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TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
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Several groups of researchers have linked perception to neural oscillations or synchrony (here called ‘fast’ temporal codes because both have to do with precise timing relationships of action potential firing between neurons). It appears, in fact, that both can be observed in gustatory neural structures. Local field potentials recorded from GC reveal high-amplitude spike-and-wave activity in the 7–12 hz range (Simon, personal communication). This phenomenon, however, appears to reflect neither oral rhythms nor taste processing; rather, experimenter-applied taste stimuli appear to halt these oscillations for however long it takes the animal to process and consume the fluid.
A number of studies have now shown taste-specific cross-correlations between pairs of
cortical (Nakamura and Ogawa, 1997;
Yokota and Satoh, 2001;
Katz et al., 2002) or
brainstem (Adachi et al.,
1989;
Di Lorenzo and Monroe, 1997) neurons.
Those studies examining pairs of neurons separated by <100 µm have revealed
synchrony, and have been interpreted in terms of common ascending influences and spatial,
columnar-like processing in GC (Yokota and Satoh,
2001). GC neurons separated by much greater distances may also fire in a
coherent fashion as well, but this phenomenon is poorly described as
synchrony—instead, it appears that at a broad spatial scale taste neurons will
change their firing rates together, but that the timing of specific action potentials are
stochastic (Katz et al.,
2002). Thus, it appears that fast dynamics may play a local role in taste
processing, and that ‘slower’ temporal coding may have an independent
function at the level of whole-system processes.
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‘Slow’ temporal codes: firing rate dynamics |
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TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
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Such a conclusion accords with the work of computationally minded researchers studying a range of systems, many of whom have questioned the evidence for temporal coding in precise times of action potentials (Shadlen and Newsome, 1998
;
Baker and Lemon, 2000), instead
suggesting that time-varying firing rates may be more closely associated with stimulus
processing (Seidemann et al.,
1996;
Oram et al., 1999). Recent
exciting work in the taste field has similarly suggested that information-rich temporal
codes in the brainstem function at the time-scale of shifting firing rates (Di Lorenzo and Victor, 2003). According to these
analyses of NTS neuron taste responses, spike time shifts interfere with
discriminability, but only if the shift is larger than 200 ms; this work is consistent
with findings described above concerning GC cross-correlations (Katz et al., 2002). In my own analysis of single
GC neurons, I have found further evidence that taste-specific information exists in
firing-rate dynamics (Katz et al.,
2001). Not only can valuable gustatory information be found in temporal
codes, in addition this information appears to evolve: in the first 100 ms following
taste administration, GC coding is purely chemosensory, but in the next second it
develops a palatability-specific quality (Katz
et al., 2001). This, together with preliminary evidence collected in
my lab, suggests that the temporal codes in GC may reflect the transformation of a
perceptual code into an action code.
These musings suggest a possible distinction that could be made between brainstem and
cortical taste activity. It is known that brainstem neurons respond more robustly to
tastants than do cortical neurons (e.g.
Nishijo and Norgren, 1997;
Katz et al., 2001); perhaps
this is because cortical neurons only fleetingly engage in stimulus processing, and then
turn their energies to using experience-generated plasticity in the transformation of
stimulus to response.
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Conclusion |
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TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
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Clearly, the investigation of temporal coding in taste is still new, and much remains to be done. As is frequently noted, rats are capable of producing basic behavioral responses to tastes with relatively little neural machinery (Grill and Norgren, 1978b
), and are able to respond
extremely quickly in some situations (Halpern and
Tapper, 1971). While it is possible that only the early portions of brainstem
responses are ‘important’ for tasting (perhaps later parts of the responses
are important solely for peculiarly human processes related to gourmet enjoyment of
flavors!), it is also possible that the importance of temporal coding in gustatory cortex
is revealed in more complex uses of taste stimuli, and that the known cortical
involvement in experience-dependent processing of tastes (Berman and Dudai, 2001) will prove to be accompanied by
changes in the temporal codes that support early responses.
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