Precis
We are beginning to understand why humans ingest so much salt. Here we address three issues: The first is whether our salt appetite is similar to that in animals, which we understand well. Our analysis suggests that this is doubtful, because of important differences between human and animal love of salt. The second issue then becomes how our predilection for salt is determined, for which we have a partial description, resting on development, conditioning, habit, and dietary culture. The last issue is the source of individual variation in salt avidity. We have partial answers to that too in the effects of perinatal sodium loss, sodium loss teaching us to seek salt, and gender. Other possibilities are suggested. From animal sodium appetite we humans may retain the lifelong enhancement of salt intake due to perinatal sodium loss, and a predisposition to learn the benefits of salt when in dire need. Nevertheless, human salt intake does not fit the biological model of a regulated sodium appetite. Indeed this archetypal ‘wisdom of the body’ fails us in all that has to do with behavioral regulation of this most basic need.
Why do humans seek salt so? The notion that the ‘wisdom of the body’ directs us to acquire specific nutritional needs is vacuous except for sodium. Sodium appetite is the only proven innate behavioral mechanism for acquiring a specific nutrient molecule – other than thirst, its physiological Siamese twin (Fitzsimons, 1998; Rozin and Schulkin, 1990). However, all we know about sodium appetite is gleaned from animal research, and whether the human predilection for salt stems from the same biological source has not garnered serious consideration. That question is relevant to how to control sodium intake in the face of its toxicity on the one hand, and the dangers of its deficiency on the other. With recent findings it has become relevant to how our lifelong craving may be initiated very early on, and whether it predicts cardiovascular vulnerability and predicates individual prescription for regulation of sodium intake. It is relevant to understand how individual differences in salt appetite arise, how palatability and pleasure may rest upon a biological rationale, and it is relevant in considering how a taste preference, largely habitual and fairly inconsequential in the individual, has had such a comprehensive influence on commerce since prehistory, and today is such a threat to public health.
Few animals pick and choose their diet. Most fulfill their nutritional needs with a single or restricted range of foods: certain eucalyptus leaves for koala, grasses for herbivores, meat for carnivores. However, very many terrestrial animals, possibly excepting the carnivores, share a predilection for sodium (Schulkin, 1982, 1984, 1991; Smedley and Eisner, 1995, 1996). Our love of sodium additionally classes us humans with the vast majority of mammals, the vegetarians, which, although they have a restricted diet, possess an innate ability to regulate their sodium requirements by means of physiological husbandry and behavioral avidity. More specifically yet, humans are classed with a tiny group of omnivores that select, study, and vary their diet in a continual effort to compose their nutritional palette, inter alia, with sodium (Rozin and Schulkin, 1990).
Sodium is an irreplaceable ion of the solute base of living organisms and of the functioning and communication of cells. Life cannot be sustained if bodily sodium levels are not maintained, and animals dwelling in domains where sodium needs to be foraged are endowed with a robust sodium appetite, first recognized, studied and described by Curt Richter, founder of our science over 70 years ago (Denton, 1982; Epstein, 1990; Richter, 1956; Schulkin, 1991, 2005).
The essentials of such a sodium appetite are its innate origins, investment in seeking salt, consumption in excess of bodily need, and dramatic physiological, behavioral and ingestive responses to sodium deficit that conserve and redistribute bodily sodium reserves, impel the animal to rummage its memory and ecology for locations of sodium, to prioritize its forage by increasing its palatability, and to rapidly ingest it when found, at any high concentration, and as sodium partnered to virtually any radical (Coldwell and Tordoff, 1996; Denton, 1982; Epstein, 1990; Richter, 1956; Schulkin, 1991; Smedley and Eisner, 1995, 1996; Schulkin, 1991; Wolf, 1969).
Sodium appetite is described by a number of characteristics: The response to sodium deficit is recognized as a crucial component of the appetite, and is often termed a sodium ‘hunger’ because it is a response to a bodily deficit, and in order to distinguish it from ‘need-free’, or spontaneous, sodium intake. Sodium hunger is for life-saving crisis intervention. In the rat the brain substrates of sodium appetite are in place within 24 h of birth (Denton, 1982; Epstein, 1990; Leshem and Epstein, 1989; Leshem, 1999; Schulkin, 1991).
In contrast, it has been suggested that spontaneous intake, which is in excess of immediate bodily needs, is anticipatory, serving to ensconce sodium sources in memory, and to ward off hyponatremic challenge. Furthermore, should this fail and the animal nevertheless experiences a sodium deficiency, the spontaneous appetite will be enduringly enhanced, as redoubled protection against a now proven hazard (Dietz et al., 2006; Epstein, 1990; Falk, 1966; Fessler, 2003; Leshem et al., 2004; Rowland and Fregly, 1988; Sakai et al., 1987, 1989; Schulkin, 1991), albeit not invariably (Leshem et al., 2004; McCaughey et al., 1996).
The spontaneous avidity that natriuphilic animals display may similarly bear the traces of sodium deficit occurring perinatally as a long-term enhancement of its palatability (Arguelles et al., 1999; Galaverna et al., 1995; Leshem, 1999; Leshem et al., 1996, 1998; Nicolaidis et al., 1990; Vijande et al., 1996), In many animals, including primates, the palatability of salt varies inversely with its availability to the body (Blair-West et al., 1998; Denton, 1982, 1991; Schulkin et al., 1984; Denton et al., 1993), and palatability is believed to be the device linking bodily deficit to appetitive behavior (Denton, 1982, 1991; Dietz et al., 2006; Berridge et al., 1984; Berridge and Schulkin, 1989; Epstein, 1991; Johnson and Thunhorst, 1997; McCaughey and Scott, 1998; Rozin and Schulkin, 1990; Schulkin, 1982, 1991; Tindell et al., 2006; Yeomans et al., 2000, 2004).
A coherent physiological model of the determinants of salt intake in laboratory rodents has emerged, including the notion that acute activation of the brain renin–angiotensin system conjointly with peripheral aldosterone, as by sodium deficit, can induce immediate, and possibly enduring, increases in sodium ingestion (Epstein, 1986, 1991; Fitzsimons, 1998; Fluharty and Epstein, 1983; Krause and Sakai, 2007; Sakai et al., 1987, 1989; Schulkin, 1991; Sakai et al., 2007; Shade et al., 2002; Weisinger et al., 1996), likely involving changes in dendritic morphology, neurochemistry, and neural activity (Contreras, 1977; Contreras et al., 1984; De Gobbi et al., 2007; De Oliveira et al., 2008; Geerling and Loewy, 2008; Jacobs et al., 1988;McCaughey and Scott, 1998; Na et al., 2007; Nachman and Pfaffmann, 1963; Roitman et al., 2002; Tamura and Norgren, 1997). Brain tachykinins and oxytocin down-regulate the appetite (Flynn, 2006; Massi et al., 1992; Stricker and Verbalis, 1990). Its anatomical infrastructure includes the circumventricular organs and tissue in their vicinity, a contribution from the amygdala and its mineralocorticoid receptors, and from executive functions by frontal regions (Geerling and Loewy, 2008; Krause and Sakai, 2007; Ma et al., 1993; Sakai et al., 1996, 2007; Schulkin, 1991; Schulkin et al., 1989). Much of this scheme is also known from the sheep, as are some differences (Denton et al., 1984a; May et al., 2000; Weisinger et al., 1980), and from the pigeon (Massi and Epstein, 1987, 1990).
Once ingested, the digestive fate of sodium is equally unique. Unlike most other ingesta, which are converted to generic matter, stored, accessed and reprocessed at need, sodium, rapidly and unaltered, takes up its various life-sustaining roles, and when required, its restorative powers are swift (Siegel, 2007; Valentine, 2007; Verbalis, 1990; Verbalis et al., 2007).
Sodium is an element of the universe, it cannot be synthesized; ingestion or injection are the sole means of replenishment. Nor are there passive stores of sodium in the body, but by a miracle of contradiction, sodium levels are regulated in blood to within some 2% of 137 mmol, while simultaneously large quantities of the ion can be lost. This is orchestrated by the kidney and its adrenal cap, their respective enzyme and mineralocorticoid secretions cascading throughout the body to juggle blood vessel diameter, heart rate, sodium flux across cell membranes, and molecular filters in kidney to jettison water appropriately, all to maintain the sodium concentration immutable in our blood.
Sodium leaks routinely from our bodies in urine, feces, and perspiration, but its loss can be catastrophic, overwhelming its controls, in dehydration, diarrhea, hemorrhage, or adrenal pathology, leading to mental and physiological derangement, and death by hyponatremia.
Hence, the beauty of sodium appetite as a matter of study stems from its patent adaptive significance, the unequivocal definition, to the ion, of the object of these adjustments, the mystery of how a naive animal recognizes the remedy to its specific hyponatremic affliction by taste, the biological prescience to rapidly complete the connection between the malaise of sodium deficit, the enhanced palatability it primes, the previously learned location of salt, and relief or cure, and finally, to consolidate this sequence enduringly in readiness for a recurring challenge.