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
 |
Why temporal coding? |
|---|
 Top Why temporal coding? ‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
|---|
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.
|
‘Fast’ temporal codes—oscillations and synchrony |
|---|
|
TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
|---|
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.
|
‘Slow’ temporal codes: firing rate dynamics |
|---|
|
TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
|---|
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.
|
Conclusion |
|---|
|
TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
|---|
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.
|
References |
|---|
|
TopWhy temporal coding?‘Fast’ temporal...‘Slow’ temporal...ConclusionReferences |
|---|
Adachi, M., Ohshima, T., Yamada, S. and Satoh, T. (1989) Cross-correlation analysis of taste neuron pairs in rat solitary tract nucleus. J. Neurophysiol., 62, 501–509.
Baker, S.N. and Lemon, R.N. (2000) Precise spatiotemporal repeating patterns in monkey primary and supplementary motor areas occur at chance levels. J. Neurophysiol., 84, 1770–1780.
Berman, D.E. and Dudai, Y. (2001) Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science, 291, 2417–2419.
Christensen, T.A., Pawlowski, V.M., Lei, H. and Hildebrand, J.G. (2000) Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat. Neurosci., 3, 927–931.[CrossRef][ISI][Medline]
deCharms, R.C. and Merzenich, M.M. (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature, 381, 610–613.[CrossRef][Medline]
Di Lorenzo, P.M. and Monroe, S. (1997) Transfer of information about taste from the nucleus of the solitary tract to the parabrachial nucleus of the pons. Brain Res., 763, 167–181.[CrossRef][ISI][Medline]
Di Lorenzo, P.M. and Victor, J.D. (2003) Taste response variability and temporal coding in the nucleus of the solitary tract of the rat. J. Neurophysiol., 90, 1418–1431.
Eckhorn, R. (1994) Oscillatory and non-oscillatory synchronizations in the visual cortex and their possible roles in associations of visual features. Prog. Brain Res., 102, 405–426.[ISI][Medline]
Friedrich, R.W. and Laurent, G. (2004) Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. J. Neurophysiol., 91, 2658–2669.
Grill, H.J. and Norgren, R. (1978a) The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res., 143, 263–279.[CrossRef][ISI][Medline]
Grill, H.J. and Norgren, R. (1978b) The taste reactivity test. Ii. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats. Brain Res., 143, 281–297.[CrossRef][ISI][Medline]
Halpern, B.P. and Tapper, D.N. (1971) Taste stimuli: quality coding time. Science, 171, 1256–1258.
Hatsopoulos, N.G., Ojakangas, C.L., Paninski, L. and Donoghue, J.P. (1998) Information about movement direction obtained from synchronous activity of motor cortical neurons. Proc. Natl Acad. Sci. USA, 95, 15706–15711.
Katz, D.B., Simon, S.A. and Nicolelis, M.A. (2001) Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J. Neurosci., 21, 4478–4489.
Katz, D.B., Simon, S.A. and Nicolelis, M.A. (2002) Taste-specific neuronal ensembles in the gustatory cortex of awake rats. J. Neurosci., 22, 1850–1857.
Lundy, R.F., Jr and Norgren, R. (2004) Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J. Neurophysiol., 91, 1143–1157.
MacLeod, K., Backer, A. and Laurent, G. (1998) Who reads temporal information contained across synchronized and oscillatory spike trains? Nature, 395, 693–698.[CrossRef][Medline]
Nakamura, T. and Ogawa, H. (1997) Neural interaction between cortical taste neurons in rats: a cross-correlation analysis. Chem. Senses, 22, 517–528.
Nishijo, H. and Norgren, R. (1997) Parabrachial neural coding of taste stimuli in awake rats. J. Neurophysiol., 78, 2254–2268.
Oram, M.W., Wiener, M.C., Lestienne, R. and Richmond, B.J. (1999) Stochastic nature of precisely timed spike patterns in visual system neuronal responses. J. Neurophysiol., 81, 3021–3033.
Seidemann, E., Meilijson, I., Abeles, M., Bergman, H. and Vaadia, E. (1996) Simultaneously recorded single units in the frontal cortex go through sequences of discrete and stable states in monkeys performing a delayed localization task. J. Neurosci., 16, 752–768.
Shadlen, M.N. and Newsome, W.T. (1998) The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J. Neurosci., 18, 3870–3896.
Smith, D.V. and Li, C.S. (2000) GABA-mediated corticofugal inhibition of taste-responsive neurons in the nucleus of the solitary tract. Brain Res., 858, 408–415.[CrossRef][ISI][Medline]
Steinmetz, P.N., Roy, A., Fitzgerald, P.J., Hsiao, S.S., Johnson, K.O. and Niebur, E. (2000) Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature, 404, 187–190.[CrossRef][Medline]
Travers, J.B. and Norgren, R. (1986) Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat. Behav. Neurosci., 100, 544–555.[CrossRef][ISI][Medline]
Yokota, T. and Satoh, T. (2001) Three-dimensional estimation of the distribution and size of putative functional units in rat gustatory cortex as assessed from the inter-neuronal distance between two neurons with correlative activity. Brain Res. Bull., 54, 575–584.[CrossRef][ISI][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||