Patricia M. Di Lorenzo

Quality Time: Representation of a Multidimensional Sensory Domain through Temporal Coding

Receptive fields of sensory neurons in the brain are usually restricted to a portion of the entire stimulus domain. At all levels of the gustatory neuraxis, however, there are many cells that are broadly tuned, i.e., they respond well to each of the basic taste qualities (sweet, sour, salty, and bitter). Although it might seem that this broad tuning precludes a major role for these cells in representing taste space, here we show the opposite—namely, that the tastant-specific temporal aspects (firing rate envelope and spike timing) of their responses enable each cell to represent the entire stimulus domain. Specifically, we recorded the response patterns of cells in the nucleus of the solitary tract (NTS) to representatives of four basic taste qualities and their binary mixtures. We analyzed the temporal aspects of these responses, and used their similarities and differences to construct the taste space represented by each neuron. We found that for the more broadly tuned neurons in the NTS, the taste space is a systematic representation of the entire taste domain. That is, the taste space of these broadly tuned neurons is three dimensional, with basic taste qualities widely separated and binary mixtures placed close to their components. Further, the way that taste quality is represented by the firing rate envelope is consistent across the population of cells. Thus, the temporal characteristics of responses in the population of NTS neurons, especially those that are more broadly tuned, produce a comprehensive and logical representation of the taste world.

Corticofugal influence on taste responses in the parabrachial pons of the rat

Abstract Although the anatomy of centrifugal input to gustatory neural structures has been described, little is known of the physiological mechanisms that convey this influence or of their functional significance. As a first step in the investigation of these issues, the effect of a reversible lesion in the gustatory neocortex (GN) on the neural code for taste in the parabrachial nucleus of the pons (PbN) was studied in rats. Electrophysiological responses to taste stimuli bathed over the tongue were recorded from single units in the PbN before, after and following recovery from an infusion of procaine-HCl into the GN. Test stimuli consisted of sapid solutions of NaCl (0.1 M), HCl (0.01 M), sucrose (0.5 M), Na-saccharin (0.004 M) and quinine-HCl (0.01 M). Infusions of procaine into the GN were correlated with both specific and nonspecific effects on the responsitivity to gustatory stimuli in the PbN. Specific effects included: (1) changes in the magnitude of response to some tastants, but not others, in a given PbN unit, (2) changes in the across unit patterns produced by sweet stimuli and (3) the appearance of OFF responses in a subset of PbN units. Nonspecific effects were evidenced by changes in the spontaneous rates of activity and by enhancement or suppression of responses across all the tastantts tested in a subset of PbN units. Comparison of these results with reports on the effects of decerebration suggests that some of these effects may be accounted for by interruption of the descending input from the GN to the PbN. In addition, the stimulus-specific effects that were noted following procaine infusion into the GN provide support for the suggestion that the GN specifically modifies the electrophysiological patterns that are evoked by salient taste stimuli.

Taste responses in the parabrachial pons of male, female and pregnant rats

Sex-related and pregnancy-related variations in taste preferences have long been known to exist in humans as well as animals. However, the neurophysiological underpinnings of these variations have not yet been described. In an effort to discover whether differences in hormonal state are reflected in the neural processing within the gustatory system, electrophysiological responses to representatives of the 4 basic taste qualities were recorded in the parabrachial nucleus of the pons (PbN) of male, diestrous female and pregnant rats. Results revealed that PbN units in female and pregnant rats showed larger responses to sweet stimuli than units in male rats. Also, a greater proportion of units in female and pregnant rats were classified as sweet-best compared with units in males. This result may correlate with the greater preference for sweet stimuli in female rats compared with males that has been reported in the behavioral literature. Analysis of response profiles with multidimensional scaling techniques showed that units that responded best to a given stimulus were placed near that stimulus for units from males, but not for units from female and pregnant rats. Hierarchical cluster analysis of response profiles suggested 3 clusters of units within each group of PbN units. Response profiles within clusters showed different types of units in male, female and pregnant rats. Collectively, these data suggest that ovarian hormones may act to alter the central processing of gustatory information. Evidence for both activational and organizational effects of ovarian hormones on the gustatory system is discussed.

Temporal coding in the gustatory system.

Early investigations of temporal coding in the gustatory system showed that the time course of responses in some neurons showed systematic differences across the various classes of taste stimuli, implying that the temporal characteristics of a response can convey information about a taste stimulus. Studies of temporal coding in the gustatory system have grappled with several unique methodological challenges, including the quantitative description and comparison of temporal patterns as well as the assessment of the relative contributions of spatial and temporal coding to the information contained in a response to a tastant. Other investigations have suggested that the cooperative activity among synchronously firing ensembles of taste-responsive neurons at all levels of processing in the brain can convey information about taste quality (sweet, sour, salty, bitter and umami). Behavioral studies using patterned electrical stimulation of the brain in awake animals have supported the idea that temporal coding of taste stimuli may have functional significance.

Taste responses in the parabrachial pons of ovariectomized rats

Since the early 1970s it has been known that female rats prefer higher concentrations of sweet stimuli compared with males. Recent data have revealed that electrophysiological responses to sweet tastes recorded in the parabrachial nucleus of the pons (PbN), the second relay in the neural pathway for taste, are larger in diestrus female rats compared with those in males. Because it has been shown that ovariectomized rats have lowered preferences for saccharin compared with intact females, it is possible to predict that responses to sweet stimuli in the PbN of ovariectomized rats might be smaller than those in intact females. To investigate this hypothesis, electrophysiological responses to representatives of the 4 basic taste qualities, i.e., salty, sour, sweet and bitter, were recorded in the PbN of ovariectomized rats. Gustatory stimuli included NaCl (0.1 M), HCl (0.01 M), sucrose (0.5 M), quinineHCl (0.01 M) and Na-saccharin (0.004 M). Comparison of taste responses of 49 PbN units in ovariectomized rats with those in the PbN of intact female and male rats showed that responses to sweet stimuli were of comparable magnitude to those in female rats but elevated compared with those in male rats. However, responses of PbN units to quinine appeared to be larger in ovariectomized rats compared with those in the PbN of both intact female and male rats. These results suggest that decreased saccharin preference in ovariectomized rats may reflect a greater sensitivity to the bitter components of the taste of saccharin. Moreover, these data provide evidence that taste responses in the PbN are influenced by both the activational and organizational actions of ovarian hormones.

Temporal coding of sensation: Mimicking taste quality with electrical stimulation of the brain

Two experiments suggested that the temporal pattern of a taste response in the brain can convey meaningful information. In Experiment 1, rats avoided lick-contingent electrical stimulation of the nucleus of the solitary tract (NTS; the first synaptic relay for taste) when the temporal pattern of pulses mimicked the electrophysiological response to quinine, but not when the temporal pattern was randomized. In Experiment 2, rats avoided lick-contingent electrical stimulation of the NTS that mimicked the temporal pattern of a sucrose response following stimulation-illness pairings. This aversion generalized to sucrose but not to the other tastants; extinction of the aversion to electrical stimulation also extinguished the aversion to sucrose. Results replicate and extend previous findings (P. M. Di Lorenzo & G. S. Hecht, 1993).

The neural code for taste in the brain stem: Response profiles

In the study of the neural code for taste, two theories have dominated the literature: the across neuron pattern (ANP), and the labeled line theories. Both of these theories are based on the observations that taste cells are multisensitive across a variety of different taste stimuli. Given a fixed array of taste stimuli, a cells particular set of sensitivities defines its response profile. The characteristics of response profiles are the basis of both major theories of coding. In reviewing the literature, it is apparent that response profiles are an expression of a complex interplay of excitatory and inhibitory inputs that derive from cells with a wide variety of sensitivity patterns. These observations suggest that, in the absence of inhibition, taste cells might be potentially responsive to all taste stimuli. Several studies also suggest that response profiles can be influenced by the taste context, defined as the taste stimulus presented just before or simultaneously with another, under which they are recorded. A theory, called dynamic coding, was proposed to account for context dependency of taste response profiles. In this theory, those cells that are unaffected by taste context would provide the signal, i.e., the information-containing portion of the ANP, and those cells whose responses are context dependent would provide noise, i.e., less stimulus specific information. When singular taste stimuli are presented, noise cells would provide amplification of the signal, and when complex mixtures are presented, the responses of the noise cells would be suppressed (depending on the particular combination of tastants), and the ratio of signal to noise would be enhanced.

Transfer of information about taste from the nucleus of the solitary tract to the parabrachial nucleus of the pons.

In the study of the neural code for gustation, the relative sensitivity of a cell to a variety of taste stimuli is defined as its response profile. To study the construction of response profiles from incoming signals, electrophysiological responses to NaCl, HCI, quinine-HCl, sucrose and Na saccharin were recorded simultaneously in pairs of single cells: one in the nucleus of the solitary tract (NTS) and the other in the parabrachial nucleus of the pons (PbN), respectively the first and second synapses in the central pathway for gustation. Of 37 units recorded in the NTS and 32 in the PbN, 12 (32%) pairs showed evidence of functional connectivity. Although PbN responses were significantly larger than those in the NTS in general, no amplification of NTS activity was apparent among those units that were functionally connected. Analysis of NTS-PbN connectivity patterns suggests that PbN units receive input from NTS units with response profiles that are both similar and different from their own pattern of sensitivities. Further analysis suggests that the stimulus-selectivity of the response profile of a PbN unit may be determined by stimulus-selective input from NTS cells that show similar response profiles. However, input from NTS cells with response profiles different from their own appears to be non-stimulus-selective. Analysis of the organization of response profiles in the two structures suggests that the cells in both the NTS and PbN cannot be easily distinguished by their patterns of sensitivity to taste stimuli.

Water as an independent taste modality

To qualify as a “basic” taste quality or modality, defined as a group of chemicals that taste alike, three empirical benchmarks have commonly been used. The first is that a candidate group of tastants must have a dedicated transduction mechanism in the peripheral nervous system. The second is that the tastants evoke physiological responses in dedicated afferent taste nerves innervating the oropharyngeal cavity. Last, the taste stimuli evoke activity in central gustatory neurons, some of which may respond only to that group of tastants. Here we argue that water may also be an independent taste modality. This argument is based on the identification of a water dedicated transduction mechanism in the peripheral nervous system, water responsive fibers of the peripheral taste nerves and the observation of water responsive neurons in all gustatory regions within the central nervous system. We have described electrophysiological responses from single neurons in nucleus of the solitary tract (NTS) and parabrachial nucleus of the pons, respectively the first two central relay nuclei in the rodent brainstem, to water presented as a taste stimulus in anesthetized rats. Responses to water were in some cases as robust as responses to other taste qualities and sometimes occurred in the absence of responses to other tastants. Both excitatory and inhibitory responses were observed. Also, the temporal features of the water response resembled those of other taste responses. We argue that water may constitute an independent taste modality that is processed by dedicated neural channels at all levels of the gustatory neuraxis. Water-dedicated neurons in the brainstem may constitute key elements in the regulatory system for fluid in the body, i.e., thirst, and as part of the swallowing reflex circuitry.

The neural code for taste in the nucleus of the solitary tract of the rat: effects of adaptation

Adaptation of the tongue to NaCl, HCl, quinine or sucrose was used as a tool to study the stability and organization of response profiles in the nucleus of the solitary tract (NTS). Taste responses in the NTS were recorded in anesthetized rats before and after adaptation of the tongue to NaCl, HCl, sucrose or quinine. Results showed that the magnitude of response to test stimuli following adaptation was a function of the context, i.e., adaptation condition, in which the stimuli were presented. Over half of all taste responses were either attenuated or enhanced following the adaptation procedure: NaCl adaptation produced the most widespread, non-stimulus-selective cross-adaptation and sucrose adaptation produced the least frequent cross-adaptation and the most frequent enhancement of taste responses. Adaptation to quinine cross-adapted to sucrose and adaptation to HCl cross-adapted to quinine in over half of the units tested. The adaptation procedure sometimes unmasked taste responses where none were present beforehand and sometimes altered taste responses to test stimuli even though the adapting stimulus did not itself produce a response. These effects demonstrated a form of context-dependency of taste responsiveness in the NTS and further suggest a broad potentiality in the sensitivity of NTS units across taste stimuli. Across unit patterns of response remained distinct from each other under all adaptation conditions. Discriminability of these patterns may provide a neurophysiological basis for residual psychophysical abilities following adaptation.