DC electrical stimulation of the pretectal thalamus and its effects on the feeding behavior of the toad (Bufo bufo)

DC Electrical Stimulation of the Pretectal Thalamusand Its Effects on the Feeding Behaviorof the Toad (Bufo bufo)

James McConville,* Peter R. Laming

School of Biology and Biochemistry, MBC, Queens University of Belfast, Belfast BT9 7BL,United Kingdom

Received 20 September 2006; accepted 5 January 2007

ABSTRACT: The feeding motivation of the com-

mon European common toad (Bufo bufo) can be quanti-

fied by the feeding sequence of arousal-orientation-

approach-fixate-snap. Previous work has found that the

optic tectum is an important structure responsible for

the mediation of feeding behaviors, and combined elec-

trical and visual stimulation of the optic tectum was

found to increase the animals feeding behaviors. How-

ever, the pretectal thalamus has an inhibitory influence

upon the optic tectum and its lesion results in disinhib-

ited feeding behaviors. This suggests that feeding behav-

ior of anurans is also subject to influence from the

pretectal thalamus. Previous studies involving the appli-

cation of DC stimulation to brain tissue has generated

slow potential shifts and these shifts have been impli-

cated in the modulation of the neural mechanisms

associated with behavior. The current study investigated

the application of DC stimulation to the diencephalon

surface dorsal to the lateral posterodorsal pretectal

thalamic nucleus in Bufo bufo, in order to assess effects

on feeding motivation. The application of DC stimula-

tion increased the incidence of avoidance behaviors to a

visual prey stimulus while reducing the prey catching

behavior component of approach, suggesting that the DC

current applied to the pretectum increased the inhibition

upon the feeding elements of the optic tectum. This can

be explained by the generation of slow potential shifts.

' 2007 Wiley Periodicals, Inc. Develop Neurobiol 67: 875–883, 2007

Keywords: Bufo bufo; direct current; feeding;

pretectum; motivation

INTRODUCTION

The feeding behaviors of anurans follow the set se-

quence of ‘arousal-orientation-approach-fixate-snap’

(Eibl-Eibesfeldt, 1951) and the number of times each

component is displayed can be used as a measure-

ment of the animal’s motivation to feed. Of particular

importance to feeding motivation is the presentation

of the ‘worm-like’ visual stimulus (WLS), since the

stomach content of toads (Bufo bufo) have revealed

that these animals feed primarily on beetles, milli-

pedes, slugs, and earthworms (Porter, 1972). This

suggests that objects moving in the same direction as

their longest edge are considered as prey, whereas

movement in the direction of the shortest edge consti-

tutes non-prey and does not elicit a prey catching

response and may even elicit a defensive reaction

(Ewert, 1987). This was verified by presentation of

small elongate artificial prey objects moving in the

same direction as their longest edge, which elicited

feeding behaviors in Hyla arborea, Rana temporaria,Alytes obstetricans, Bufo bufo bufo, Bufo bufo spino-sus, and Bombina variegata, while objects moving

perpendicular to the longest edge did not elicit feed-

ing behaviors and even induced avoidance behaviors

(Ewert, 1969)

Visual input in anurans is integrated by the optic

tectum and has been extensively investigated by AC

Correspondence to: J. McConville ([email protected])

' 2007 Wiley Periodicals, Inc.Published online 21 February 2007 in Wiley InterScience (www.interscience.wiley.com).DOI 10.1002/dneu.20390

875

stimulation (Roitbak et al., 1992) and presentation of

visual stimulation (Laming and Ewert, 1984a; Ewert,

1989; Laming et al., 1995; McConville et al., 2006).

Within the optic tectum, the nature of visual objects

is determined primarily through the activity of the

tectal T5 cells consisting of the T5 (1), T5 (2), and T5

(3) subtypes. T5 (1) subunits respond maximally to

objects moving in the same direction as its longest

edge and T5 (3) subunits respond maximally to exten-

sion perpendicular to movement. However, T5 (2)

subunits integrate and interpret visual input in that

they are sensitive to both types of objects (Laming,

1992). These prey selective cells also have input to

the medulla via tecto-bulbar tracts, suggesting that

they have a major influence upon response generation

(Satou and Ewert, 1984).

There is also a close cellular relationship between

the optic tectum and the pretectal thalamus (Szekely

and Lazar, 1976; Wilczynski and Northcutt, 1983a,b;

Schwippert et al., 1995) in that the pretectal thalamus

exerts a degree of inhibition upon the optic tectum

(Ewert, 1974, 1983, 1989; Ewert et al., 1979, 1983;

Buxbaum-Conradi and Ewert, 1995) as shown by

disinhibited feeding induced by pretectal thalamic

lesions (Laming and Ewert, 1982). Disinhibition of

feeding behavior by pretectal lesions largely involves

the prey selective tectal T5 (2) cells, since prectecal

lesion also results in increased firing rate and de-

creased selectivity of the T5 (2) cells (Ewert, 1967,

1968; Ewert et al., 1974; Laming and Ewert, 1982).

The pretectal inhibition is generated by the activity of

TH3 cells within the pretectal thalamus, which are

analogous to the non-prey sensitive tectal T5 (3) cells

in that they are maximally responsive to non-prey

objects (Ewert et al., 1983).

The present investigation aims to determine if DC

stimulation of the diencephalon surface just dorsal to

the lateral posterodorsal thalamic nucleus (Lpd) has

an effect on toads’ (Bufo bufo) feeding behavior.

Applied AC and DC electrical current to the anuran

optic tectum results in ionic fluxes recorded as slow

potential shifts (SPS) (Roitbak et al., 1987, 1992;

Laming, 1992; Laming et al., 1992; Sterritt et al.,

2000) and there is a wealth of knowledge suggesting

that SPS’s have a significant impact on neural

function. This is because SPS reflect movement of

potassium ions through glial cells which modulate

neuronal function with obvious implications for

behavior (Ransom, 1973a,b,c; Laming, 1983, 1989,

2000; Laming et al., 1984a,b, 1995; Roitbak et al.,

1987, 1992).

Compared to that on AC stimulation, relatively

little work has been conducted on the behavioral

effects of DC stimulation applied to brain structures

especially on the anuran pretectal thalamus, but

previous investigations have found that DC stimula-

tion applied to the surface of brain tissue induces

SPS’s (Sterritt et al., 2004). This induction of ionic

fluxes through glial cells may be done without neces-

sarily stimulating neurons, giving a purer reflection

of the effects of SPS’s.

This current study found that as the current applied

increased feeding behaviors decreased and avoidance

behaviors increased when presented with a prey like

object. The stimulation may be having an effect on

the TH3 cells/cell populations in the pretectal thala-

mus associated with visual stimulus recognition via

generation of SPS’s, increasing inhibition upon the

prey selective functions of the optic tectum.

METHODS

Animals

Adult toads (Bufo bufo) obtained from a commercial

supplier were maintained in vivaria for at least a month

prior to the experiment, being fed twice a week on meal-

worm (Tenebrio molitor) larvae. Ten male toads were

selected for experimentation and all experiments and

animal conditions were subject to the Animals (Scientific

Procedures) Act 1986.

Behavioral Testing

Toads were placed on a 20 3 20 cm2 crystallizing dish

painted white apart from 10-cm transparent window. The

dish was placed in the center of a box with a turntable under

a fixed base to allow a piece of black cardboard 3 cm long

3 0.75 cm to be rotated around the dish at �2 cm/s as a

‘worm like’ stimulus (WLS). The WLS could then be pre-

sented both clockwise and anti-clockwise around the dish,

i.e., left to right and right to left, respectively, from the

toad’s perspective. The box measured 40 3 40 3 40 cm3,

and the inside was painted white to give a homogeneous

background and optimal contrast (McConville et al., 2006),

see Figure 1.

Electrode Preparation

Teflon-coated platinum Iridium wire of 0.0125 mm diame-

ter was cut into 2.5 cm lengths. One end of the wire was

heated in a flame until a �1-mm ball formed. The other end

was gently scraped with a razor blade to remove a �1 cm

length of the Teflon insulation all around the wire. A length

of 0.6-mm diameter resin insulated copper lead also had a

similar length of the resin insulation scrapped off and the

two wires were then twisted together at these insulation free

points and soldered together to form a stimulation lead

(Fig. 2).

876 McConville and Laming

Developmental Neurobiology. DOI 10.1002/dneu

Two of these leads were then twisted together to form a

lightweight cable of two electrodes and fashioned into a he-

lix. Above the experimental box a supporting horizontal

length of wire was suspended with a swivel attached. To

this the copper cable and ball electrode assembly was fixed

vertically, and the electrodes were surgically fixed to the

cranium; see Figure 1.

Operations

Toads were anesthetized by ether inhalation until breathing

ceased and were covered with a moist tissue to aid cutane-

ous respiration. The temperature of the room was thermo-

statically controlled at (15 6 1)8C. The skin overlying the

cranium was removed using fine curved scissors and the

cranium over the diencephalon was thinned by buffing

the surface with a dental burr to make a transparent

window. This allowed the position of the surface overlying

the lateral posterodorsal thalamic nucleus (Lpd) to be

checked before drilling. A �2 mm diameter burr hole was

drilled over the Lpd/Thalamus surface and ball electrodes

were placed in the hole making contact with the thalamus

surface and secured to the skull with a drop of Permabond

adhesive. The electrode delivering positive polarity DC

stimulation always contacted the right side of the thalamus

overlying the Lpd (Fig. 3). A layer of tissue paper soaked

with water covered the base of the crystallizing dish and the

toad was placed in the dish and allowed to recover for 24 h.

Electrode positioning was verified by examining the brain

post mortem, whereby the cranium was carefully removed

and the proximity of the burr hole to the thalamus surface

determined.

Experiments

Ten animals were used to assess the effects of DC currents.

A Grass photoelectric stimulus isolation unit (PSIU6) fitted

to a Grass S44 stimulator provided the DC stimulation. The

order of all possible current strength and WLS direction

configurations (two per individual current strength) were

presented randomly to reduce order effects with the excep-

tion of zero current, which was always first and the highest

current, which was always given last. This meant that each

toad was subject to 14 stimulation events. DC current was

applied for 10 s while the WLS passed the window of the

dish and the remote presentation of the visual stimulus was

�2 s after initiation of the DC current. The stimulation

events were separated by a 5-min interstimulus period. The

DC stimuli were 0, 0.1, 1, 10, 50, 100, and 300 lA. The

current range applied was chosen to cover a large range of

stimulation while remaining low in order to reduce the pos-

sibility of tissue damage. Sterrit et al. (2004) applied 1 mV

of DC stimulation to induce slow potential shifts in the toad

optic tectum. The magnitude of the SPS’s were greatly

reduced in the posterior tectum compared to anterior

records, which were nearer the stimulation electrode. Ranck

(1975) found that 55–80 lA AC stimulation elicited neuron

responses at a maximum distance of 1090 lm. Quick and

Laming (1988) used similar techniques to asses the current

spread of applied pulsed currents ranging from 0.1 to

200 lA to the surface of the goldfish telencephalon and

optic tectum and found that the maximum distance at which

current spread would excite tectal neurons was a longditudi-

nal distance of 95.5 6 11.16 lm.

The animal’s behavior was observed by the experimenter

from above the testing arena. This was deemed appropriate

since this was the normal method by which the animals

were fed in the vivarium prior to testing.

The results were analyzed by the multivariate analysis

of variance technique (MANOVA) using the statistical

package for the social sciences (SPSSx) (SPSSx Inc., 1986).

Figure 1 Experimental chamber (Laming, 1992). [Color

figure can be viewed in the online issue, which is available

at www.interscience.wiley.com.]

Figure 2 Electrode preparation. [Color figure can be viewed in the online issue, which is available

at www.interscience.wiley. com.]

Pretectal Thalamus and Feeding Behavior 877


The Pillais trace calculation was used for averaged multivar-

iate tests of significance. These calculations are denoted in

the form PF (df1, df2) ¼ F, p ¼ sig, where df1 and df2 are

the numerator and denominator, respectively. From this the

variables responsible for the significance of the multivariate

test (Pillais) was determined by univariate F-tests, denoted

by F (df1, df2) ¼ F, p ¼ sig. SPSSx. Averaged univariate F-

tests are defined by Avf (df1, df2) ¼ X, p ¼ sig, where df1and df2 are the numerator and denominator, respectively.

The number of times each behavior was observed

per 10-s stimulation event constituted the ‘Response Fre-

quency.’ The following behaviors were observed and found

to be statistically significant.

1. Arousal: Nondirectional elevation of the head and

extension of the forelimbs.

2. Approach: Actual movement of the animal towards

the WLS.

3. Retreat: Backwards moving away from the WLS.

4. Crouch: Lowering of head and shoulders.

5. Misdirected orientation/approach: Orientation and/

or approach in the opposite direction of the WLS

propagation.

RESULTS AND ANALYSIS

The effect of current within subjects averaged multi-

variate tests of significance were significant [PF

(36, 324) ¼ 2.6, p < 0.001] and this was attributed to

arousal [F (6, 54) ¼ 2.9 p < 0.05] (Fig. 4), approach[F (6, 54) ¼ 2.7, p < 0.05] (Fig. 5), retreat [F (6, 54)

¼ 23.1, p < 0.001] (Fig. 6), and crouch [F (6, 54) ¼18, p < 0.001] (Fig. 7).

When behaviors were analyzed individually, aver-

aged test of significance involving current within

subjects effects also found that arousal [Avf (6, 54)

¼ 2.9, p < 0.05] (Fig. 4), approach [Avf (6, 54) ¼2.7, p < 0.05] (Fig. 5), retreat [Avf (6, 54) ¼ 23.1,

p < 0.001] (Fig. 6) and crouch [Avf (6, 54) ¼ 18,

p < 0.001] (Fig. 7) were all significant.

Increased DC stimulation elicited a mostly constant

arousal response albeit with a decrease at 0.1 and

50 lA (Fig. 4). Increased DC stimulation decreased

the approach response up until a stimulation of

300 lA, where there is a small increase in response

frequency (Fig. 5). The retreat and crouch responses

were not evident at currents less than 100 lA but

increased between 100 and 300 lA (see Figs. 6 and 7,

respectively). The figures show bar graphs of the

mean response frequency of each behavior and asso-

ciated þ standard error mean (SEM) bars per 10-s

stimulation event.

DISCUSSION

DC stimulation of the dorsal surface of the lateral

posterodorsal thalamic nucleus (Lpd) in Bufo bufo

Figure 4 Every stimulation event generated the arousal

response albeit with much lower values at 0.1 and 50 lA.

[Color figure can be viewed in the online issue, which is

available at www.interscience.wiley.com.]

Figure 3 The position of the frontal telencephalon, cen-

tral diencephalon over Lpd, and rear optic tectum (Laming,

1992). [Color figure can be viewed in the online issue,

which is available at www.interscience.wiley.com.]



results in a relatively constant arousal response and a

decrease in the frequency of the ‘approach’ feeding

behavior, albeit with an increase at 300 lA and this

may be evidence of a novel behavior to predators.

The increase in the approach response at 300 lA may

be evidence of some initial precursory movements

associated with responses to predators in which toads

will sometimes freeze and turn towards snakes and

expose their flanks in a stiff legged stance (Ewert and

Traud, 1979).

On the other hand, increased DC stimulation

increased the frequency of the avoidance behaviors,

‘retreat’ and ‘crouch’. This suggests a shift in how

the animal is interpreting the visual stimulus in that at

higher DC current the prey like visual stimulus is

being interpreted as predatory at the expense of feed-

ing behavior.

The optic tectum is the primary integrative center

of visual input in anurans, where a number of tectal

cells interpret and process visual information. ‘T5’

cell types within the optic tectum and its three sub-

types are primarily responsible for the interpretation

of moving visual objects to determine if they are prey

or non-prey (Ewert et al., 1979, 1983; Ewert, 1983,

1987). T5 (3) cells respond maximally to visual stim-

uli moving perpendicular to its longest edge, i.e., an

antiworm stimulus and T5 (1) cells respond maxi-

mally to visual stimuli moving parallel to its longest

edge and movement perpendicular to the longest

edge, i.e., both worm like and non-worm configura-

tions (Ewert et al., 1979, 1983; Ewert, 1983, 1987).

The T5 (2) cells represent a functional unit of visual

stimulus perception as they respond maximally to

prey like configurations and since T5 (2) cells can be

antidromically stimulated from the medulla the T5

(2) cells translate the processed sensory information

to motor activity via the tecto/bulbar tracts (Satou

and Ewert, 1984).

The pretectal thalamus has a significant input to

the optic tectum (Wilczynski and Northcutt, 1983a,b),

which has an inhibitory influence upon the prey selec-

tive elements of the optic tectum as seen by disinhib-

ited feeding responses resulting from pretecal lesions

(Ewert, 1967, 1968; Ewert et al., 1974; Laming and

Ewert, 1982). Within the pretectal thalamus ‘TH3’

cells respond primarily to large moving stimuli and

are found predominantly in the Lpd and lateral poste-

rior (P) pretectal regions. Since the pretectal neuropil

receives retinal input from a number of retinal

Figure 6 An increase in current intensity results in an

increase in the retreat response frequency. The behavior is

not displayed at all at currents less than 100 lA. [Color fig-

ure can be viewed in the online issue, which is available at

www.interscience.wiley.com.]

Figure 5 Increased DC stimulation decreases the ap-

proach response. [Color figure can be viewed in the online

issue, which is available at www.interscience.wiley.com.]



ganglion cells, such visual input would activate the

TH3 cells, increasing their activity and as a result the

inhibitory output to the tectum (Ewert, 1987, 1989;

Schwippert et al., 1995).

AC electrical stimulation of the pretectal thalamus

temporarily inhibits the activity of the prey selective

tectal T5 (2) cells, which proves that electrically

induced increases in activity of the pretectal thalamus

inhibits the prey selective function of the optic tectum

(Ewert et al., 1974).

There is also an inhibitory influence from the

telencephalon upon the pretectal thalamus as shown

by ablation of the telencephalon, resulting in feeding

behaviors failing to occur, whereas subsequent pre-

tectal ablation results in disinhibited feeding behav-

iors (Ewert, 1968, 1987). A striato-pretecto-tectal

feedback loop via the lateral forebrain bundle (LFB)

and lateral anterior thalamus provides a neural basis

for a more global modulation of the feeding behavior

of amphibians (Wilczynski and Northcutt, 1983a,b).

Matsumoto et al. (1991) examined intracellular re-

cordings from the Lpd/P region of the pretectal thala-

mus in response to electrical stimulation of the caudal

ventral striatum (vSTR) or ipsilateral LFB. The study

found pure IPSP’s from the striatum to the Lpd/P as

previously suggested by ablation studies. A more

recent work by Buxbaum-Conradi and Ewert (1995)

investigated the activity of the caudal ventral striatum

(vSTR) in visuomotor activity of Bufo marinus. A

number of striatal cell types were defined in terms of

responses to visual and electrical stimulation of the

LFB. The study found that 40% of the responses to

LFB stimulation were striatal efferents and this could

innervate the optic tectum by striato-pretecto, striato-

tegmento, and/or striato-pallio-pretecto-tectal path-

ways. This suggests that the vSTR may also be modu-

lating the perceptual and motor aspects of amphibian

visual attention.

The present study was conducted to determine the

effects of pretectal DC stimulation upon the anuran

feeding behaviors, since relatively little work had

been undertaken with direct current, with most work-

ers employing AC stimulation. To our knowledge, no

work had been undertaken using simultaneous DC

stimulation of the anuran pretectal thalamus and pre-

sentation of prey like objects. The results of the pres-

ent study suggest that increased DC stimulation

increased the activity of the Lpd region of the pretectal

thalamus, increasing the inhibitory input to the prey

selective processes in the optic tectum. This increased

inhibition on the optic tectum resulted in increased

avoidance behavior at the expense of feeding or prey

catching behaviors to the visual stimulus and the WLS

being interpreted as non-prey or predator. The precise

mechanisms of how DC stimulation produced this

shift in motivation are not clear from the current study

but previous studies using DC electrical stimulation of

anuran brain tissue generated slow potential shifts

(SPS) (Sterritt et al., 2004). SPS’s are a manifestation

of the depolarizing movement of potassium ions

through glial cells (King, 1960; Ransom and Goldring,

1973b,c; Gardner-Medwin, 1983, 1987; Laming,

1983, 1989, 2000; Laming and Ewert, 1984a,b; Roit-

bak et al., 1992) and there is evidence that SPS polarity

and amplitude are associated with changes in motiva-

tional state in many species (Laming, 1983, 1992,

2000; Laming and Ewert, 1984a,b; Quick and Laming,

1990; Laming et al., 1995).

Neuron resting potentials are dependent on lower

extracellular potassium concentrations, and propagat-

ing action potentials are a depolarization of the

neuron membrane with expulsion of potassium into

the extracellular milieu. Increased extracellular potas-

sium reduces neuronal firing thresholds by depolariz-

ing the membrane close to that required for the gener-

ation of action potentials priming cells and increasing

the likelihood of action potential generation (Laming,

1983, 2000; Laming and Ewert, 1984a). Application

of potassium to the brain resulted in an increase in

the unit and SPS responses from the optic tectum of

Figure 7 An increase in current intensity results in an

increase in the crouch response frequency. The behavior is

not displayed at all at currents less than 100 lA. [Color fig-

ure can be viewed in the online issue, which is available at

www.interscience.wiley.com.]



non-hungry toads to a square visual stimulus (Laming

and Laming, 2004).

In mammals the SPS closely matches the reloca-

tion of potassium by astrocytic glia, suggesting that

astrocytic movement of potassium ions is responsible

for the recorded SPS. Glial cells readily take up

potassium, and since neurons expel potassium during

action potential generation, these ions will be taken

up by the surrounding glia. The potassium ions will

then flow through the glial cells along concentration

gradients to be expelled into regions of extracellular

space of comparatively lower ion concentration, i.e.,

areas of relatively lower neuronal activity (Gutnick,

et al., 1981; Gardner-Medwin, 1983, 1987; Roitbak

et al., 1987, 1992). Gap junctions between astrocytes

offer a pathway of reduced resistance to ion flow,

making it possible for the potassium to flow through

glia and down concentration gradients faster than

action potentials can propagate across synapses

(Gutnick et al., 1981; Gardner-Medwin, 1983, 1987).

In addition, glial cells and neurons engage in an inti-

mate physiological relationship during cell maturation

(King, 1960; Rakic, 1974; Hatten, 1990; Cameron

and Rakic, 1994). The preservation of these ontogenic

relationships results in a ‘functional syncytium,’

where relocation of potassium may ‘prime’ function-

ally related populations of neurons, offering a poten-

tial mechanism of modulation of motivation through

the relocation of potassium to cells in imminent

receipt of input before the input arrives.

Anuran brain tissues have considerably less astro-

cytes but are heavily invested with radial glia, which

are long single processes and these glial cells offer

a similar low resistance pathway to ions and may

account for the SPS recorded at depth and across

anuran brain tissues (Laming, 1983, 1992, 2000; Lam-

ing and Ewert, 1984a,b; Roitbak et al., 1992; Laming

et al., 1995; Laming and Laming, 2004; Sterritt et al.,

2004).

Experiments by Laming and Ewert (1984a) carried

out on conscious but immobilized toads elicited

monophasic SPS responses as well as visual unit and

EEG responses to simulated natural prey objects. At

the tectal surface, the unit activity preceded EEG and

SPS changes, but in the deeper layers of the sensory

processing system, the SPS preceded the EEG change

and significantly pre-empted the activity of the local

units, suggesting a faster transfer of potassium ions

through radial glia, than action potential propagation

(Laming and Ewert, 1984a).

Investigations involving the application of DC

stimulation to anuran brain surface tissues have also

elicited SPS’s. Sterritt et al. (2004) applied DC stimu-

lation to the surface of the optic tectum of toads

(Bufo bufo) as well as presenting visual prey like

object similar to those presented here. The anterior

tectum is the primary input area for the optic tectum

and negative SPS responses from the anterior tectum

reflected the animal’s prior motivation to feed. This

negative SPS was associated with a positive SPS in

the posterior tectum and the movement of the animals

resulted in a reversal of polarity, suggesting that

movement itself activates large swathes of the tectum

and activates many sinks and sources of potassium

both tangentially and radially through the optic

tectum (Laming et al., 1995; Sterritt et al., 2004). DC

stimulation of the optic tectum also resulted in SPS

responses of similar polarity and rebound responses

as with visual stimulation albeit of a greater magni-

tude. The SPS were generated by the DC stimulation

and summated with the SPS associated with the prior

feeding motivation to enhance the neuronal

responses, especially with the negative phase of the

SPS (Sterritt et al., 2004). Experiments have also

been conducted by applying DC stimulation to the

optic tectum of toads, which increased feeding

responses and avoidance responses, suggesting a

more global activation of neuronal cells and potas-

sium sinks (McConville, 2006). Experiments apply-

ing DC stimulation to the scalp in humans affects

cortical activity and even improves learning func-

tions, and this may well be due to the modulatory

effects of SPS’s (Nitsche and Paulus, 2000; Nitsche

et al., 2002; Marshall et al., 2004).

In the current situation, DC stimulation-induced

SPS’s may be relocating potassium ions, via radial

glia, to layers of the pretectal thalamus housing the

non-prey selective TH3 cells before the onset of the

local neuronal response. Priming of these cells prior

to input would increase their likelihood of action

potential generation and at a population level increase

the inhibitory output to the prey selective elements

of the optic tectum. This may well account for the

increase in avoidance behaviors to prey like objects

evidenced in the current study.

REFERENCES

Buxbaum-Conradi H, Ewert JP. 1995. Pretecto-tectal

influences—What the toads pretectum tells its tectum:

Antidromic stimulation/recording study. J Comp Physiol

176:169–180.

Cameron RS, Rakic P. 1994. Identification of membrane

proteins that comprise the plasmalemal junction between

migrating neurons and radial glial cells. J Neurosci 14:

3038–3055.

Eibl-Eibesfeldt I. 1951. Nahrungserwerb und Beuteschema

der Erdkrote (Bufo bufo). Behaviour 4:1–34.



Ewert JP. 1967. Untersuchungen uber die Anteile zentral-

nervoser Aktionen an der taxisspezifischen Ermundung

beim Beutefang der Erdkrote (Bufo bufo). Zeitschrift Fur

Vergleichende Physiologie 57:263–288.

Ewert JP. 1968. Der Einflub von Zwisschenhirndefekten

auf die Visuomotorik im Beute-und Fluchtverhalten

der Erdkrote (Bufo bufo). Zeitschrift Fur Vergleichende

Physiologie 61:41–70.

Ewert JP. 1969. Quantatative analyses von reiz-reaktions-

beziehungen bei visullem auslosen der Beutefang-

Wenderreaktion der Erdkote (Bufo bufo L). Pflugers Arch

ges Physiol 308:225–243.

Ewert JP. 1974. The neural basis of visually guided be-

haviour. In: Held R, editor. Recent Progress in Percep-

tion. Readings in Scientific American. San Francisco, CA:

Freeman, pp 96–104.

Ewert JP. 1983. Tectal functions underlying prey-catching and

predator avoidance behaviors in toads. In: Vanegas H,

editor. Neurology of the Optic Tectum. New York: Plenum,

pp 247–416.

Ewert JP. 1987. Neuroethology of releasing mechanisms:

Prey catching in toads. Behav Brain Sci 10:337–405.

Ewert JP. 1989. The release of visual behaviour in toads:

Stages of parallel/hierarchical information processing.

In: Ewert JP, Arbib MA, editors. Visuomotor Coordi-

nation, Amphibians, Comparisons, Models, and Robots.

New York: Plenum, pp 39–109.

Ewert JP, Borchers HW, Weitersheim AV. 1979. Direc-

tional sensitivity, invariance and variability of tectal T5

neurons in response to moving configurational stimuli in

the toad (Bufo bufo). J Comp Physiol 131:191–201.

Ewert JP, Burghagen H, Schurg-Pfeiffer E. 1983. Neuroe-

thological analysis of the innate releasing mechanism

for prey-catching behaviour in toads. In: Ewert JP,

Capranica R, Ingle D, editors. Advances in Vertebrate

Neuroethology. London: Plenum, pp 413–475.

Ewert JP, Hock FJ, Weitersheim AV. 1974. Thalamus/

Praetectum/Tectum: Retinale Topographie und phy-

siolische Interaktionen bei der Krote (Bufo bufo). J Comp

Physiol 92:333–346.

Ewert JP, Traud R. 1979. Releasing stimuli for antipredator

behaviour in the common toad (Bufo bufo L). Behaviour

68:170.

Gardner-Medwin AR. 1983. Analysis of potassium dy-

namics in mammalian brain tissue. J Physiol 325:383–

426.

Gardner-Medwin AR. 1987. Assessment of the glial spatial

buffer mechanism in rat brain, frog brain and retina. In:

Roitbak AI, editor. Functions of Neuronglia. Tiblisi, USSR:

Metsniereba press, pp 137–145.

Gutnick MJ, Connors BW, Ransom BR. 1981. Dye coupling

between glial cells in the guinea pig neocortical slice.

Brain Res 213:486–492.

Hatten ME. 1990. Riding the glial monorail: A common

mechanism for glial-guided neuronal migration in differ-

ent regions of the developing mammalian brain. Trends

Neurosci 13:179–184.

King JG. 1960. Comparative investigation of neuroglia in

representative vertebrates. J Morph 119:434–466.

Laming GE, Laming PR. 2004. Tectal responses to potas-

sium loads and subsequent visual stimuli are affected by

motivational state in the toad. Bufo bufo. Comp Biochem

Physiol A 137:665–674.

Laming PR. 1983. Relationship between the responses of vis-

ual units, EEGs and slow potential shifts in the tectum of

the toad Bufo bufo. In: Ewert JP, Capranica RR, Ingle DJ,

editors. Advances in Vertebrate Neuroethology. London:

Plenum, pp 595–603.

Laming PR. 1989. Do glia contribute to behaviour? A

neuromodulatory review. J Comp Physiol 94:555–568.

Laming PR. 1992. Information processing and neuromodu-

lation in the visual system of frogs and toads. Network

3:71–88.

Laming PR. 2000. Potassium signalling in the brain: Its role

in behaviour. Neurochem Int 36:271–290.

Laming PR, Ewert JP. 1982. The effects of pretectal lesions

on neuronal, sustained potential shifts and EEG respon-

ses of the toads tectum to presentation of a visual stimu-

lus. Comp Biochem Physiol A 76:247–252.

Laming PR, Ewert JP. 1984a. Visual unit, EEG and

sustained potential shift responses to biologically signifi-

cant stimuli in the brains of toads (Bufo bufo). J Comp

Physiol 154:89–101.

Laming PR, Ewert JP. 1984b. Visual unit, EEG and sus-

tained potential shift responses in the brains of toads

(Bufo bufo) during alert and defensive behaviour. Physiol

Behav 31:463–468.

Laming PR, Ocherashvili IV, Nicol AU. 1992. Dendritic

and sustained shifts in potential to electrical stimulation

of the anuran tectal surface. Comp Biochem Physiol A

101:91–96.

Laming PR, Ocherashvili IV, Nicol AU, Roughan JV,

Laming BA. 1995. Sustained potential shifts in the toad

tectum reflect prey catching and avoidance behaviour.

Behav Neurosci 109:150–160.

Marshall L, Molle M, Hallschmid M, Born J. 2004. Trans-

cranial direct current stimulation during sleep improves

declarative memory. J Neurosci 24:9985–9992.

Matsumoto N, Schwippert WW, Beneke TW, Ewert JP.

1991. Forebrain-mediated control of visually guided

prey-catching in toads: Investigation of striato-pretectal

conncetions with intracllular recording/labelling meth-

ods. Behav Processes 25:27–40.

McConville JR, Sterritt L, Laming PR. 2006. Behavioural

responses to electrical and visual stimulation of the toad

tectum. Behav Brain Res 170:15–22.

Nitsche MA, Liebetanz D, Tergau F, Paulus W. 2002. Mod-

ulation of cortical excitability in man using transc-

ranial direct current stimulation. Nervenarzt 73: 332–

335.

Nitsche MA, Paulus W. 2000. Excitability changes induced

in the motor cortex by weak transcranial direct current

stimulation. J Physiol 527:633–639.

Porter KR. 1972. Herpetology. Philadelphia: WB Saunders.

Quick IA, Laming PR. 1988. Cardiac, ventillatory and

behavioural arousal responses evoked by electrical brain

stimulation in the goldfish (Carassius aurarus). Physiol

Behav 43:715–727.



Quick IA, Laming PR. 1990. Relationship between ECG,

EEG and SPS responses during arousal in the goldfish

(Carassius auratus). J Comp Physiol A 95:459–471.

Ranck JB. 1975. Which elements are excited in electrical

stimulation of mammalian central nervous system: A

review. Brain Res 98:417–440.

Ransom BR, Goldring S. 1973a. Ionic determinants of

membrane potential of cells presumed to be radial glia in

cerebral cortex of cat. J Neurophysiol 36:855–868.

Ransom BR, Goldring S. 1973b. Slow depolarisation in

cells presumed to be radial glia in cerebral cortex of cat.

J Neurophysiol 36:869–878.

Ransom BR, Goldring S. 1973c. Slow hyperpolarisation in

cells presumed to be radial glia in the cerebral cortex of

the cat. J Neurophysiol 36:879–892.

Rakic P. 1974. Emergence of neuronal and glial cell lineages

in primate brain. In: Black IB, editor. Cellular and Molec-

ular Biology of Neuronal Development. New York:

Plenum, pp 28–50.

Roitbak AI, Fanardjhyan VV, Melkonyan DS, Melkonyan

AA. 1987. Contribution of radial glia and neurons to the

surface negative potentials of the cerebral cortex during

its electrical stimulation. Neurosci 20:1057–1067.

Roitbak AI, Ocherashvili IV, Laming PR, Roitbak TA.

1992. Stimulus evoked sustained potential shifts and

changes in extracellular potassium concentration of the

frog optic tectum. J Comp Physiol 170:317–323.

Satou M, Ewert JP. 1984. Specification of tecto-motor

outflow in toads by antidromic stimulation of tecto-

bulbar-spinal pathways. Naturwissenschaften 71:52.

Schwippert WW, Beneke TW, Ewert JP. 1995. Pretecto-

tectal influences B—How retinal and pretectal inputs to

the toads superficial tectum interact: A study of electri-

cally evoked field potentials. J Comp Physiol 176:181–

192.

Sterritt L, Laming G, Laming PR. 2004. Neuronal responses

are differentially affected by the polarity of tectal DC

stimulation in the toad (Bufo bufo). Comp Biochem

Physiol 138:467–474.

Szekely G, Lazar GY. 1976. Cellular and synaptic architec-

ture of the optic tectum. In: Llinas R, Precht W, editors.

Frog Neurobiology. Berlin: Springer, pp 297–385.

SPSSx Inc. 1986. Statistical Package for the Social Scien-

ces. New York: McGraw Hill.

Wilczynski W, Northcutt RG. 1983a. Connections in the

bullfrog striatum: Efferent projections. J Comp Neurol

214:333–343.

Wilczynski W, Northcutt RG. 1983b. Connections of the

bullfrog striatum: Afferent connections. J Comp Neurol

214:321–332.



Documents

DC electrical stimulation of the pretectal thalamus and its effects on the feeding behavior of the toad (Bufo bufo)