and its practical implications
by E.R. Ørskov
It is prudent in a discussion of conditioned responses to draw attention to the originator of the concept (Pavlov, 1927), who defined it as follows:
“Conditioned reflexes are phenomena of common and widespread occurrence. Their establishment is an integral function in everyday life. We recognize them in ourselves and in other people or animals under such names as habits and training and all of these are really nothing more than the result of an establishment of new nervous connexions during the post-natal existence of the organism.”
That these reflexes could influence nutrition was also established by Pavlov (1902), who is mainly credited with experiments on conditioned salivation in dogs but who also established an effect on other digestive glands.
E.R. ørskov is with the Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB, Scotland.
Conditioned responses in ruminants with direct nutritional relevance
Conditioned responses and their relevance to practical nutrition are much less well documented than, for instance, adaptive responses to changes in nutrition or changes in temperature and endocrinological state. Experimental proof of a direct influence of higher centres on digestive secretion requires quite sophisticated techniques, but a conditioned response of a similar nature has no doubt been observed for as long as lactating ruminants have been hand milked or machine milked. This relates to the process of milk release, which is influenced to a large extent by extraneous stimuli. Stimulating receptors by massaging the udder is not necessarily required provided the surrounding routine, stockmen, noise of milking utensils, etc., signal unequivocally the milking time. On the other hand, stimulation of nerve receptors in the udder is not always sufficient to achieve milk release. A negative reaction to a new stockman or other interfering signals can inhibit it. The example of milk let down to illustrate conditioning is used here because the effect of the release of milk can be readily observed. Stimuli which in the same manner exhibit an effect on digestion are equally or even more important, but they can only be directly measured by sophisticated techniques.
Conditioning of gastric secretion in ruminants
While the original observations on dogs were made many years ago by Pavlov, similar observations on ruminants are of more recent date. Much has been contributed to our knowledge on this subject by researchers at Melbourne. Carr, McLeay and Titchen reviewed this work in 1970. McLeay and Titchen (1970) showed that acid secretion in the abomasum was increased when sheep were given the stimuli associated with feeding time but not fed. D.H. Carr and D.A. Titchen (unpublished report) observed changes in salivary secretion in sheep when teased with food and when the regular animal attendant walked past the animal room. A very interesting observation was made by D.A. Titchen and L.M. McLeay (personal communication): they encountered a profound reduction in gastric secretion in a sheep when one particular person was talking in the corridor not far from the animal room.
Conditioning of the motility of the digestive tract
In a similar manner to conditioning of secretion in the digestive tract there is now considerable evidence that gut motility is very sensitive to extraneous stimuli. Such evidence was discussed by Mielke (1961), and evidence of conditioning affecting intestinal motility (Ruckebusch, 1963a)and reticulo-rumen movement (Ruckebusch, 1963b) has been presented and referred to also by Carr et al. (1970).
When a liquid is infused into the upper oesophagus it will normally enter the rumen
Conditioning of the oesophageal groove reflex
The recent work on the nature of the reflex responsible for the closure of the oesophageal groove is of considerable interest, not only because it has now been well documented but because it is a reflex which can have a considerable and direct influence on the course of digestion, since it is the means by which young animals convey liquids direct to the abomasum, by-passing the rumen.
When Ørskov and Benzie (1969) reported their work on this subject, they were essentially in agreement with Watson (1944), who concluded that “the passage to the abomasum of liquids sucked by the lamb is not determined by the temperature or the composition of the liquid or by the posture of the animals while sucking nor by the act of sucking itself. It is the result of the actuation of the pattern of behaviour which surrounds the act of sucking.” However, Watson was also led to infer that some mechanical stimulation by the teat was involved.
This finding was in contrast to those of many earlier workers, who had concluded that such factors as chemical composition and temperature of the liquid and posture while drinking were important. In later work, however, Ørskov, Benzie and Kay (1970) did not agree with Watson on the effect of mechanical stimulation, since liquid drunk from a trough would directly by-pass the rumen in the same manner as that taken from a teat. The proof that the oesophageal groove was conditionable was provided when it was shown that liquid infused into the oesophagus distal to the nerve receptors in the mouth and pharynx associated with groove closure (Comline and Titchen, 1951) entered the abomasum in animals when the external stimuli signalled feeding time. When no such signals were given liquids infused in this manner always entered the rumen.
Confirmative data were obtained by Newhook and Titchen (1974), who showed that markers placed in the lips of the oesophageal groove were seen by radiography to move when lambs were teased, thus indicating groove closure. This was also observed in unpublished work by the author and R.N.B. Kay. The observation that the oesophageal groove was never closed when the motive for drinking was to quench thirst was confirmed by Ørskov and Benzie (1969), and this fact has important consequences in the management of systems in which it is desired to feed part of the diet in such a way that the rumen is by-passed (Ørskov, 1972a, 1972b).
When a liquid is infused into the upper oesophagus in a lamb stimulated by the sight of the bottle from which it normally drinks, it will enter the abomasum, thus showing conditioning of groove closure
Feeding systems in which the rumen is by-passed
The fact that water consumed to quench thirst enters the rumen is extremely important, because it means that only if the two motives for drinking (drinking for thirst and drinking in a state of juvenile excitement) are clearly separated is it possible to successfully utilize the oesophageal groove in the functioning ruminant. While this may sound a complicated rule to observe, it can be simply followed by ensuring that the animals have unrestricted access to drinking water and that the liquid suspension which is intended to bypass the rumen is given in restricted quantities as a continuation of the milk-feeding regime. The latter rule, of course, implies that such systems must be based on artificial rearing and that feeding ad lib on milk substitutes is likely to extinguish the reflex in some animals (Lawlor et al., 1971). The time of weaning from their dam is quite critical; the earlier the animals are weaned the easier it is to train them to drink from a teat or a trough. Delaying weaning to after two to three weeks of age will result in a large proportion of the animals failing to adapt successfully to the new feeding system.
It does not follow that the lambs or calves will, for instance, refuse to drink milk but they will not drink with any sign of excitement or pleasure. In such animals, most of the liquid consumed can be expected to have entered the rumen. Even when weaned at birth an animal occasionally fails to show the normal behaviour while drinking. Such animals are usually in poor condition and almost invariably the milk given will have entered the rumen.
Method of drinking
As mentioned earlier, the method of drinking (sucking from a teat or drinking from a bowl or trough) is not important for successful closure of the oesophageal groove. It is worth pointing out, however, that while trough feeding has obvious advantages as far as management is concerned, this regime has some disadvantages when one liquid is replaced by another, for instance milk replaced by a protein suspension. The new diet must be introduced very gradually to the trough-fed animals, since a strange smell can lead to refusal to drink (E.R. Ørskov and Thivend, unpublished results). In practice it may be advisable to include about 5 percent milk substitute in the suspension offered after weaning. A change to a new diet with teat feeding is usually not recognized by the animals.
Concentration of liquid suspension
The dry matter concentration in the liquid suspension drunk is not critical. The main requirement seems to be that it must be sufficiently liquid to allow swallowing without further incorporation of saliva. An attempt was made by G. Wenham and the author to investigate this by gradually decreasing the water content in milk substitute until it was given in the dry form. When the lamb had to chew and incorporate saliva to facilitate swallowing, the oesophageal groove soon ceased to function. Feeding of solid food designed to enter the rumen can be pursued independently of liquid feeding.
Retention of reflex in mature animals
Provided the reflex is being constantly reinforced (i.e., the animals are given daily or every two days or so a drink following the routine and regime to which they are accustomed), it is possible to retain the reflex in almost all of the animals. Six lactating goats at the Rowett Research Institute which have now completed five gestation periods are still being used in experiments in which the rumen is by-passed, and there seems to be no loss in efficiency of groove closure.
Motility and secretion
The fact that secretion and gastric motility are greatly influenced by extraneous stimuli means that poorly defined factors like stockmanship cannot be ignored in the handling and general care of domesticated animals.
A decreased intestinal motility can have very serious consequences for intake and digestion, and can lead to a bacterial infiltration in the small intestine with well-known results (e.g., White et al., 1969). The effect of an impaired gastric secretion on digestion and metabolism is poorly documented in animals. However, since many digestive enzymes are activated as a result of gastric secretion, an impairment will no doubt lead to inefficient digestion in the small intestine, so that a large number of substrates will reach the large intestine and give rise to scouring and dehydration. Another consequence of impaired gastric secretion is the effect of achlorhydria in the etiology of anaemia in man (e.g., Shearman et al., 1966).
Goats in their fifth lactation at their daily bottle feed
While factors influencing animal well-being may be inadequately understood, there is little doubt that the young, early-weaned ruminant, which is particularly sensitive, responds to kindness and attention like the human child, and unless good stockmanship can be provided early weaning and artificial rearing are unlikely to be successful. For all ruminant animals regular feeding times, feeding regimes, milking procedures and a regular stockman are very important factors.
As stated earlier, the effect of extraneous stimuli on gastric secretion and motility is difficult to measure. The fact that it exists raises questions with regard to the effect of new routines adopted in the intensification of animal production systems, e.g., effects of group feeding, conditions in calf houses, and so on.
The oesophageal groove
The object of the work on the oesophageal groove reflex at the Rowett Research Institute was to explore the possibility of using this mechanism as a means of by-passing the rumen with nutrients which were destroyed or partially destroyed as a result of rumen fermentation. In the young ruminant with a high level of feeding, the requirement for protein exceeds that which the microorganisms can make available by fermenting the carbohydrate. Protein supplements are, however, partly degraded in the rumen so the feeding of protein in a suspension, by-passing the rumen, could lead to a greatly increased efficiency.
Table 1. Comparison of nitrogen balance results of 11 lambs given protein supplements in liquid and dry form
|Nitrogen intake||Urinary nitrogen||Faecal nitrogen||Nitrogen retention|
|Grams per day|
|Barley + liquid protein supplement||22.9||6.5||6.6||9.8|
|Barley + dry protein supplement||22.8||8.7||6.2||7.9|
|SE of means||0.68||0.59||0.67||0.91|
Source: Ørskov and Fraser, 1969.
A comparison (Ørskov et al., 1970) of casein, fish meal and soybean meal, given either in solid form so that they entered the rumen, or in liquid form so that the rumen was by-passed, showed the efficiency of N retention from casein to be improved by 31 percent, fish meal by 27 percent and soybean meal by 24 percent. A typical example of a N balance experiment is shown in Table 1, where the effects of giving a mixed protein supplement in liquid and dry forms are compared. The urinary N excretion was significantly decreased and retention increased when the supplement was fed in the liquid form.
The oesophageal groove can, of course, be used equally well for carbohydrate-rich foods which in turn might enhance the efficiency of energy utilization, since fermentation losses in heat and methane could be avoided if the carbohydrates with alphalinked glucose polymers could be digested in the small intestine. Work on this aspect has shown that the small intestine of ruminants has a limited capacity for digestion of starch (Mayes and Ørskov, 1974) and even for glucose absorption (Ørskov et al., 1971), and no capacity for sucrose digestion (Ørskov, 1973). By-passing the rumen with lipids has some interesting implications. Lipids entering the rumen in excess of 3–5 percent of the diet will interfere with fermentation of the cellulose and thus cause low feed intake. However, the capacity for absorption of lipids in the small intestine is very great; in fact, unpublished work has indicated that ruminants will absorb energy in the form of lipids sufficient to meet their maintenance energy need.
Table 2. Effect of giving a high fat supplement (70 percent beef tallow) in dry form so that it entered the rumen, or in liquid form so that the rumen was by-passed, on voluntary intake of dried grass and total intake of digestible energy
|Supplement||Level of supplementation (% of estimated metabolizable energy intake||Intake of dried grass|
(g DM/kg Wt0.75)
|Total digestible energy|
|SE of means||2.7||0.035|
Source: Bailey and Ørskov, 1974 (reproduced by courtesy of the Nutrition Society).
Table 2 shows the effects of giving lipids so that they enter or bypass the rumen — on the voluntary intake of dried grass by lambs and on the total intake of digestible energy. Lipids entering the rumen caused reductions in intake of dried grass so that no increase in total digestible energy was achieved. On the other hand, feeding of lipids so that the rumen was by-passed did not cause a significant reduction in intake of dried grass and consequently increased the total digestible energy intake. By-passing the rumen with lipids may thus provide a means of increasing energy intake or of altering the composition of the fatty acids in meat or milk.
From the information available it would seem that the oesophageal groove could be used to advantage in the feeding of protein supplements to early weaned calves and lambs until they reach a stage of maturity at which their protein requirement is met by microbial protein. This occurs in Friesian calves at about 200 kg liveweight and in Suffolk cross lambs at about 35 kg liveweight (Ørskov, 1974). For carbohydrates, the use of the oesophageal groove has probably a restricted application owing to limitations on digestion and absorption from the small intestine. If lipids can be obtained at low prices, the oesophageal groove offers a means of taking them past the rumen with no deleterious effect on intake and digestion of roughage. Furthermore, the composition of fats given in this manner will directly influence the composition of the fatty acids laid down.
In comparision with the protection of proteins and lipids by chemical treatment (Ferguson et al., 1967; Scott et al., 1971), using the oesophageal groove has the advantage that there is no cost involved in chemical treatment and no uncertainty about over-or underprotection. It has the disadvantages that it must be based on artificial rearing, and requires restricted feeding of the liquid supplement. The choice must be based on the method that would be most suitable and economical in the production system under consideration.
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