ORIGINAL PAPER

Effects of prolonged exposure to cold on the spontaneous activityof two different types of filiform sensilla in Pyrrhocoris apterus

Ales Skorjanc • Ales Lipicnik • Kazimir Draslar

Received: 16 April 2013 / Revised: 26 June 2013 / Accepted: 15 July 2013 / Published online: 4 August 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract We recorded the spontaneous activity of T1 and

T2 filiform sensilla from October to May in Pyrrhocoris

apterus acclimatized to outdoor conditions. The aim of the

study was to determine how prolonged exposure to cold

affects two closely related mechanosensitive sensilla. We

recorded the activity at seven temperatures from 5 to

35 �C. In both sensilla types the activity level was reduced

during winter, which correlated to changes in acclimati-

zation temperature (r = 0.7), the reduction was greater at

high recording temperatures, and the effects of exposure to

cold were reversed by transferring the animals indoors.

However, T1 activity always increased monotonically, if

the recording temperature was increased from 5 to 35 �C,

whereas T2 activity in cold-acclimatized animals increased

to temperatures between 20 and 30 �C and then started

decreasing. As a result, the temperature sensitivity of the

activity was reduced more profoundly in T2 sensilla (in T2

Q10 was reduced from 3.5 in October to 1.4 in January,

whereas in T1 it was reduced from 2.5 to 2.2). In conclu-

sion, we have shown that prolonged exposure to cold does

affect filiform sensilla; however, the effect is significantly

different in the two sensilla types.

Keywords Pyrrhocoris apterus � Filiform sensilla �Mechanoreception � Cold acclimatization �Temperature sensitivity

Abbreviations

F Impulse frequency

Q10 Temperature coefficient

r Pearson coefficient of correlation

SD Standard deviation

SEM Standard error of mean

Ta Temperature of the abdomen

Introduction

The red firebug, Pyrrhocoris apterus (L.) (Heteroptera), is

one of a few species of Pyrrhocoridae family extending to

the temperate zone of the Palaearctic Region (review by

Socha 1993). In much of its habitat the firebug had to adapt

to great seasonal changes in the environmental tempera-

ture. In Central Europe it gets warmed to more than 30 �C

in the summer and cooled far below 0 �C in the winter.

Low temperatures during winter pose a particularly great

risk to the survival of the firebug, which does not tolerate

freezing. The female of the firebug starts laying eggs in

April and May. The new generation of adult animals arises

during summer. Most of them enter a facultative diapause

that delays the reproductive cycle until the next spring

(Kostal and Simek 2000). Surviving winter is therefore

crucial for the reproductive success of the firebug. It is

known that the firebug undergoes a series of physiological

changes that increase its resistance to cold. During the state

of enhanced cold-hardiness the consumption of oxygen by

the firebug and its body water content are reduced, whereas

the concentration of cryoprotective polyols in the hemo-

lymph, as well as the osmolality of the hemolymph are

increased (Kostal and Simek 2000; Kostal et al. 2001;

Slachta et al. 2002). On the level of cell membranes the

composition of phospholipids is modified (Hodkova et al.

1999, 2002; Slachta et al. 2002; Tomcala et al. 2006). We

asked here, if prolonged exposure to cold during winter

A. Skorjanc (&) � A. Lipicnik � K. Draslar

Department of Biology, Biotechnical Faculty, University

of Ljubljana, Vecna pot 111, 1000 Ljubljana, Slovenia

e-mail: ales.skorjanc@bf.uni-lj.si

123

J Comp Physiol A (2013) 199:807–815

DOI 10.1007/s00359-013-0841-7

also affects sensory systems of the firebug. This is a rele-

vant question, since the firebug remains active during

winter. On a sunny day it often crawls from the litter to the

tree trunk, where its body temperature can raise to almost

30 �C due to sun illumination, allowing a more active

behavior (Skorjanc et al. 2007). To answer the question

above, we recorded the spontaneous activity of T1 and T2

filiform sensilla from October to May in firebugs accli-

matized to outdoor conditions.

We chose the spontaneous activity as a probe for

detecting functional changes in filiform sensilla, because its

properties are in the case of the firebug well-defined. The

filiform sensillum of an insect is a sensory organ with a

single sensory neuron that detects movements of a cuticular

hair. The sensory neuron is surrounded by a few accessory

cells (review by Keil 1997). In the firebug 28 units are

located on the abdomen. They are classified into three basic

types: T1 (hair length 305–360 lm), T2 (hair length

115–165 lm) and T3 (hair length 85 lm) according to their

structural and functional properties (Draslar 1973, 1980;

Skorjanc et al. 2009). All three types are spontaneously

active, i.e., they discharge nerve impulses in the absence of

an external stimulus. Spontaneous activity is a common

property of many insect filiform sensilla (Nicklaus 1965;

Westin 1979; Buno et al. 1981; Dagan and Volman 1982;

Shimozawa and Kanou 1984; Hamon and Guillet 1994;

Landolfa and Miller 1995). It increases their sensitivity,

and in directionally sensitive sensilla sets the ‘‘zero’’ level

that is modulated up or down according to the stimulus

direction. In the firebug only type T1 is directionally sen-

sitive, whereas types T2 and T3 respond with an increase in

impulse discharge rate to a deflection of the sensory hair in

any direction from the resting position (Draslar 1973). The

level of spontaneous activity is tightly regulated in the

firebug. Different types of sensilla have different levels of

activity that range from 57 imp/s in T1 to 3.3 imp/s in T2 to

0.5 imp/s in T3 sensilla. Their spontaneous activity also

differs in some other properties, such as temperature sen-

sitivity and response to hypoxia, which has been explained

by different sources of the activity (Skorjanc et al. 2009).

Importance for stimulus encoding, different functional

properties in different sensilla types, and tightly regulated

level make spontaneous activity a parameter of choice for

studying the effects of exposure to cold on filiform sensilla.

In the previous study we compared the spontaneous

activity of type T1 sensilla at 20 �C in cold- and warm-

acclimatized animals (Skorjanc et al. 2007). We were not

able to show a significant difference between the two groups.

Further analysis of the data and additional experiments

revealed, however, that the spontaneous activity does

change. In this paper we present the results of our measure-

ments in T1 and T2 sensilla from October to May, which best

summarize our findings. We show that the level of activity

drops during cold months, which correlates to the drop in the

acclimatization temperature. Exposing the animals to indoor

conditions reverses the effect. We also show a distinct dif-

ference in the effects of cold acclimatization on the activity

of T1 and T2 sensilla, which supports the hypothesis of dif-

ferent sources of spontaneous activity in these two types, as

suggested by Skorjanc et al. (2009).

Materials and methods

Experimental animals

Adult males of the bug P. apterus (L.) (Insecta: Heteroptera)

were used in all experiments. They were collected in the

garden of Bogensperk castle near Litija, Slovenia

(46�102500N, 14�5102700E). They were maintained in glass

containers, supplied with linden seeds and water ad libitum.

Acclimatization to outdoor conditions

The study was carried out over a period of 8 months. The

spontaneous activity of filiform sensilla was recorded from

November 2006 until May 2007. Additional recordings

were made in October 2007. To ensure natural-like accli-

matization the animals were kept in glass containers out-

side the laboratory. The containers were put into a box that

was half-way buried into the ground in a protected shady

area. Openings in the box provided ventilation, whereas

transparent walls ensured the light/dark cycle. Temperature

and humidity inside the box were measured using a remote

sensor of a weather station BAR 628 HG (Oregon Scien-

tific, Oregon, USA) between 9 and 10 am. Measured

temperatures (i.e., acclimatization temperatures) are shown

in Fig. 3c (dots). They are plotted against the data for

7 am, 2 pm and mean daily air temperature in Ljubljana,

Slovenia (published by the Slovenian Environment Agency

on the internet: http://www.arso.gov.si). The relative

humidity inside the box remained high throughout the

whole experimental period, ranging between 75 and 98

percent with the mean value of 91 percent (SD 8). When

making recordings of the spontaneous activity, the animals

were exposed to indoor conditions as little as possible. The

preparation of the animals was done in \15 min, whereas

the recordings were done in 20–30 min.

Acclimatization to indoor conditions

In January and February, we transferred some of the ani-

mals from outside into the laboratory to test whether the

effects of exposure to cold could be reversed. The animals

were kept at 20 ± 2 �C and the usual laboratory light

regime. The spontaneous activity of filiform sensilla was

808 J Comp Physiol A (2013) 199:807–815

123

recorded immediately before the transfer of the animals

(day 0), and then every day for the first four successive

days after the transfer (days 1–4).

Signal recording and processing of data

The spontaneous discharge of nerve impulses was used to

study the effects of prolonged exposure to cold on filiform

sensilla. Impulses were recorded in the fifth abdominal

segment from a group of three sensilla, which belong to the

three main types T1, T2 and T3. The distances between sen-

silla were less than 100 lm, ensuring identical experimental

conditions for each individual sensillum. Impulses were

recorded extracellularly using tungsten microelectrodes

(Goodfellow, Cambridge, UK). The experimental proce-

dures were described in detail in Skorjanc et al. (2009). Here

we summarize them and describe the modifications.

Prior to the recording the thorax of the animal was

removed and the wound sealed with a nontoxic polymer

Kwik-Cast (WPI, Sarasota, USA). The preparation was fixed

with its dorsal side to a holder. In order to prevent uncon-

trolled warming of the preparation, cyanoacrylate glue was

used instead of the usual bee wax-colophony mix. The

application of the glue shortened the viability of the prepa-

ration. However, we established that the properties of sen-

silla remained unaffected for at least 5 h, which was enough

time to make a complete experiment. Recordings were per-

formed in a Faraday cage, which was covered with thick

foam to ensure still conditions and, therefore, proper spon-

taneous activity. The reference electrode was inserted into

the abdomen through the last segment. The registration

electrode was inserted approximately 0.5 mm away from

sensilla. The signals from all three sensilla units were

recorded simultaneously. They were amplified and filtered

using AI520 low-noise head-stage amplifier and CyberAmp

320 signal conditioner (Molecular Devices, USA). For data

acquisition and storage we used Power1401 interface (CED,

Cambridge, UK) and PC computer, which were controlled

with Spike2 v.6.02 software (CED, Cambridge, UK). Spike2

was used also for off-line impulse sorting and signal analysis.

To ensure the consistency of experiments we set inclusion

criteria for the preparations. The amplitude of the signal had

to be sufficient to reliably identify and sort different types of

spikes, and the signal amplitude and spike frequency had to

remain stable throughout the experiment.

The spontaneous activity was recorded at seven tem-

peratures in the range between 5 and 35 �C. The tempera-

ture was controlled with a custom made preparation holder.

The holder consisted of two copper blocks with a Peltier

element fixed between them. The temperature of the upper

block was regulated to a precision of ±0.2 �C by adjusting

the current driving the Peltier element. The temperature was

measured with a thermocouple inserted into the block (K

type, HH501DK, Omega, USA). The holder was first cooled

to 5 �C and then warmed to 35 �C in 5� steps. At each

temperature the spontaneous activity was stabilized for

3 min prior to the recording. Although the activity appears

already at 0 �C, we did not make recordings at temperatures

below 5 �C due to water condensation on the preparation.

We also did not make recordings at temperatures above

35 �C, which cause damage to the sensillum. We also

checked whether warming the preparation to 35 �C caused

any irreversible damage. After making recordings at 35 �C

we cooled the preparation back to 20 �C. Only preparations,

in which the amplitude of the signal and the level of

spontaneous activity returned back to the values recorded

prior to warming, were used for data analysis. Due to

thermal dissipation the core temperature of the animal’s

abdomen deviated from the holder temperature by approx-

imately ?3 �C at 5 �C and -3 �C at 35 �C. At the site of

sensilla a smaller temperature deviation could be expected,

because they are located close to the dorsal side of the

abdomen, which was in direct contact with the holder sur-

face. In the paper ‘‘recording temperature’’ always refers to

the temperature of the holder. The core temperature of the

abdomen was used only when calculating Q10 coefficient,

because we wanted a more precise estimation of the tem-

perature sensitivity of the spontaneous activity. The

abdominal temperature was measured in a separate set of

experiments. Q10 was calculated from impulse frequencies

at holder temperatures of 5 and 35 �C using Eq. (1):

Q10 ¼F 35 �Cð ÞF 5 �Cð Þ

� � 10 �CTa 35 �Cð Þ�Ta 5 �Cð Þ

ð1Þ

where F is impulse frequency and Ta is abdominal

temperature.

Data analysis was done using GraphPad Prism v.4.03

software (GraphPad Software, California, USA) and cus-

tom software written for Matlab r.2007b (TheMathWorks,

Natick, MA, USA). The level of spontaneous activity was

quantified as a number of nerve impulses per second [imp/

s], determined from 60 s long recordings. For comparison

of mean impulse frequencies and Q10 values in animals

acclimatized to different conditions the unpaired t test was

used. The correlation between the level of spontaneous

activity and the acclimatization temperature was quantified

using the Pearson coefficient of correlation.

Results

Acclimatization to outdoor conditions

We recorded the spontaneous activity of T1, T2 and T3

filiform sensilla from October to May in animals accli-

matized to outdoor conditions. The activity was recorded at

J Comp Physiol A (2013) 199:807–815 809

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seven temperatures from 5 to 35 �C. T1 and T2 sensilla

were spontaneously active in all preparations (Fig. 1),

whereas the activity of T3 sensilla was detected in

approximately one half of the preparations. Impulse fre-

quencies, recorded at 20 �C and averaged over all

8 months, were 54 imp/s in T1 (SD 7; n = 54), 4 imp/s in

T2 (SD 4; n = 54) and 0.2 imp/s in T3 sensilla (SD 0.3;

n = 29). Data for T3 sensilla were excluded from further

analysis due to low impulse frequency and unreliable

impulse detection, which would lead to low precision data.

During cold months the level of spontaneous activity

was decreased, but only at higher recording temperatures

(Fig. 2). In both T1 and T2 sensilla the activity was the

highest in October. In November it dropped to a level that

persisted until May, when it again increased. The drop was

greater in T2 than in T1 sensilla. The level of activity

closely followed the acclimatization temperature (Fig. 3).

We calculated the Pearson coefficient of correlation

between the mean monthly temperature inside the box,

where the animals were kept, and the mean monthly

impulse frequency. In the case of T1 sensilla the correlation

was significant at recording temperatures above 20 �C and

in the case of T2 sensilla at temperatures above 25 �C. At

30 �C the correlation coefficient was 0.7 (P = 0.04) for

both types of sensilla.

The study also revealed a significant difference

between T1 and T2 sensilla. The spontaneous activity of

T1 sensilla always increased monotonically, if the

recording temperature was increased from 5 to 35 �C. The

thermal response of T2 sensilla was more variable and

complex. In some cold adapted animals T2 activity

increased until temperatures around 20 to 30 �C were

reached. Above these temperatures it started to decrease

(Figs. 1, 2c). The decrease was not always monotonic. In

some cases the impulse frequency would first decrease,

but then increase again as the temperature was increased

even more. The relative number of T2 sensilla that

exhibited the reductive effect of the recording temperature

on the spontaneous activity at any of the 5 �C steps in the

range from 5 to 35 �C is shown in Fig. 4. In October 30

percent of T2 sensilla exhibited the reductive effect, while

in March and April all sensilla exhibited the effect. In

May there was a complete reversal in the thermal

response. The spontaneous activity of all investigated T2

sensilla increased monotonically throughout the whole

temperature range from 5 to 35 �C. As a result of the

reductive effect of high recording temperatures, the

overall temperature sensitivity of T2 spontaneous activity

was greatly reduced during winter. Q10 dropped from 3.5

(SEM 0.6, n = 7) in October to 1.4 (SEM 0.2, n = 6) in

January (P = 0.008). In comparison, the change in the

temperature sensitivity of T1 activity was much smaller.

Q10 dropped from 2.50 (SEM 0.06, n = 7) to 2.19 (SEM

0.05, n = 6); however, the drop was statistically signifi-

cant (P = 0.004).

Acclimatization to indoor conditions

During cold months the level of spontaneous activity was

reduced in both sensilla types, as shown above. In order

to test whether these effects were reversible, we trans-

ferred some of the firebugs from outside into the labo-

ratory in January and February. In the laboratory the

ambient temperature ranged from 18 to 22 �C. We

recorded the activity of T1 and T2 sensilla immediately

before the transfer (day 0) and then every successive day

for the first 4 days after the transfer (days 1 to 4). We

recorded the activity in 3–5 preparations per day. No

significant differences were observed between recordings

in January and February, hence the data for the 2 months

were pooled together.

The level of T1 and T2 spontaneous activity increased

after the transfer of the animals into the laboratory (Fig. 5).

In T1 sensilla it increased gradually in the first 2 days,

when it reached a value that persisted until the fourth day.

The level on the fourth day, recorded at 30 �C, was

Fig. 1 Recordings of spontaneous activity. Nerve impulses of T1 and

T2 filiform sensilla were recorded in animals acclimatized to outdoor

conditions in October (a) and January (b). Impulses of T1 and T2

sensilla can easily be identified (T2 impulse amplitude is always

significantly larger than T1 impulse amplitude, indicated by arrows).

On the left, temperatures, at which the recordings were made. On the

right, frequencies of nerve impulses. Note that, in January the

frequency of T2 impulses decreases, if the temperature is increased

from 25 to 35 �C

810 J Comp Physiol A (2013) 199:807–815

123

statistically the same as the one in October in animals

acclimatized to outdoor conditions (P = 0.29). In contrary

to that, the activity of T2 sensilla did not change signifi-

cantly in the first 2 days. The level of activity remained

low, exhibiting the typical reductive effect of recording

temperatures above 20 to 30 �C on the impulse frequency.

On the third day the level started to increase. In four

preparations out of five the spontaneous activity mono-

tonically increased from 5 to 35 �C. On the fourth day all

preparations exhibited similar temperature dependency.

The activity monotonically increased throughout the whole

temperature range. The mean level of activity, recorded at

30 �C, was statistically the same as the one in October in

animals acclimatized to outdoor conditions (P = 0.16).

This shows that the effects of exposure to cold on the

spontaneous activity are reversible in both sensilla types

under laboratory conditions.

Discussion

The firebug is an established species for studying cold

acclimatization in insects (review by Hodkova and Hodek

2004). A lot of effort has been put into understanding the

changes that occur in the firebug during winter. We found

that prolonged exposure to cold also affects its sensory

systems. We discuss changes in the spontaneous activity of

T1 and T2 filiform sensilla, and propose potential causes of

the observed changes.

Prolonged exposure to cold reduces spontaneous

activity

We recorded the spontaneous activity of T1 and T2 type

sensilla from October to May in animals acclimatized to

outdoor conditions. In each preparation, the activity was

Fig. 2 Spontaneous activity of

T1 and T2 filiform sensilla from

October to May. The activity

was recorded at seven

temperatures from 5 to 35 �C in

firebugs acclimatized to outdoor

conditions. a Spontaneous

activity of T1 and T2 sensilla

from October (X) to May (V).

Mean impulse frequency is

shown (nX: 7, nXI: 7, nXII: 7, nI:

6, nII: 7, nIII: 7, nIV: 7, nV: 6).

During cold months, an overall

drop in the frequency can be

observed in both types. b,

c Spontaneous activity of

individual T1 (b) and T2

(c) sensilla in October and

January. In January, the impulse

frequency of several T2 sensilla

decreases, if the preparation is

warmed above 20–30 �C. This

never occurs in T1 sensilla

J Comp Physiol A (2013) 199:807–815 811

123

recorded at seven temperatures in the range between 5 and

35 �C. We chose this range because it resembles temper-

atures experienced by the firebug in its natural environ-

ment. Extending the measurements to 8 months and

to recording temperatures above 20 �C proved to be criti-

cal. In our initial study, we could not establish a significant

difference between the spontaneous activity of T1 sensilla

recorded at 20 �C in cold- and warm-acclimatized animals

(Skorjanc et al. 2007). Comparison of the activity over a

period of 8 months, however, revealed a reduction in the

activity level of T1 and T2 sensilla during cold months. The

reduction was not observed at lower recording tempera-

tures, but became apparent at temperatures above 20 �C.

The main parameter affecting the spontaneous activity

appears to be the acclimatization temperature, which is

supported by the strong correlation between the mean

monthly acclimatization temperature and the impulse fre-

quency. Pearson correlation coefficient for the activity

recorded at 30 �C was 0.7 in both T1 and T2 sensilla.

However, other factors, such as dehydration of the animals,

should also be considered.

With the modified protocol, we also detected a significant

difference between T1 and T2 sensilla. The activity of T1

sensilla always monotonically increased, if the recording

temperature was increased from 5 to 35 �C. In contrary to that,

temperatures above 20–30 �C had a reductive effect on the

activity of T2 sensilla in cold-acclimatized animals. It should

be noted here that T1 and T2 sensilla were exposed to the same

thermal conditions during acclimatization process and during

recordings, since the distance between them is less than

100 lm. It should also be noted that their activity was recor-

ded simultaneously in the same preparation allowing a direct

comparison between the two. This proves that the difference

in the thermal response of T1 and T2 sensilla is indeed intrinsic.

As a result of the reductive effect of high recording temper-

atures on the activity of T2 sensilla, their temperature sensi-

tivity was greatly reduced. Q10 dropped from 3.5 (SEM 0.6,

n = 7) in October to 1.4 (SEM 0.2, n = 6) in January. In

Fig. 3 Relation between spontaneous activity level and acclimatiza-

tion temperature. a, b Level of spontaneous activity of T1 (a) and T2

(b) sensilla from October (X) to May (V) at 10 and 30 �C

(mean ± SEM). c Temperature inside the box, where the animals

were kept, measured between 9 and 10 am. Individual measurements

are shown by dots. Air temperatures are shown for comparison. The

mean air temperature is shown by the line, whereas the gray area

represents the difference between 7 am and 2 pm air temperature. The

spontaneous activity, recorded at 30 �C, closely follows the acclima-

tization temperature. The corresponding Pearson correlation coeffi-

cient is 0.7 (P = 0.04) for both T1 and T2 sensilla

Fig. 4 Relative number of T2 sensilla exhibiting a decrease in the

spontaneous activity at high recording temperatures. As shown in

previous figures (Figs. 1, 2), during the cold months the level of

spontaneous activity of several T2 sensilla decreases, if the prepara-

tion is warmed above 20–30 �C. The relative number of such sensilla

rises from October to April. In April, all T2 sensilla exhibit this

phenomenon. In May, however, the activity of all T2 sensilla again

monotonically increases throughout the entire range between 5 and

35 �C

812 J Comp Physiol A (2013) 199:807–815

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comparison, in T1 sensilla it dropped from 2.50 (SEM 0.06,

n = 7) to 2.19 (SEM 0.05, n = 6). Although the overall

reduction in the temperature sensitivity could be an epiphe-

nomenon of the physiological changes occurring during

exposure to cold, it could also be an adaptation of sensilla to

winter conditions. While the firebug is exposed to low tem-

peratures most of the time, it often moves from the leaf litter to

the tree trunk, where it becomes more active. There its body

temperature can rise to almost 30 �C in a matter of minutes

due to insolation, but it can also suddenly drop back to air

temperature due to wind and cloudiness (Skorjanc et al. 2007).

Lower temperature sensitivity would mean a more stable

sensory output from filiform sensilla in conditions of such

extreme temperature oscillations.

When the cold-acclimatized animals were transferred

from outside into the laboratory in January and February,

the spontaneous activity of T1 and T2 sensilla settled in less

than a week at a level comparable to the one in October.

This is in agreement with our previous studies, where we

collected the animals in their natural environment and

recorded the activity of sensilla throughout the whole year.

The animals were acclimatized to laboratory conditions

usually for more than a week prior to the recordings.

Despite the differences in their physiological state, the

spontaneous activity of filiform sensilla was always limited

to a similar, narrow range, and we never observed the

reductive effect of high recording temperatures on T2

activity (Skorjanc et al. 2009). This indicates that the

effects of exposure to cold remain reversible with the time

period of 1 week, which likely resembles the dynamics of

thermal acclimatization in nature.

Dissipation of electrochemical gradients of ions

and membrane remodeling could affect the spontaneous

activity

The spontaneous activity of mechanosensitive sensilla is

presumably generated by the receptor current flowing

Fig. 5 T1 and T2 spontaneous

activity during acclimatization

of firebugs to indoor conditions.

Firebugs were transferred from

outside into the laboratory in

January (asterisk) and February

(open circle). They were kept at

20 �C (±2 �C) and the usual

laboratory light regime. a,

b Activity of individual T1

(a) and T2 (b) sensilla,

measured before indoor

acclimatization (day 0) and after

4 days of acclimatization (day

4). c Overview of T1 and T2

activity, measured at seven

temperatures from 5 to 35 �C,

for all 4 days of acclimatization.

Note that the acclimatization

process is faster in T1 sensilla

J Comp Physiol A (2013) 199:807–815 813

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through a portion of mechanosensitive transduction channels

that are open, while the sensory hair is in the resting position

(Thurm 2001). In the firebug, exposure to low temperatures

leads to a gradual dissipation of potassium and sodium

electrochemical gradients across cell membranes (Kostal

et al. 2004). According to the model of receptor potential

generation in epidermal mechanoreceptors of insects

(Thurm 1974), the dissipation of electrochemical gradients

would directly influence the electromotive force driving the

receptor current and, consequently, the spontaneous activity

of the filiform sensillum. The activity could also be affected

by modifications in the phospholipid composition of cell

membranes occurring during cold acclimatization of the

firebug (Hodkova et al. 1999, 2002; Slachta et al. 2002;

Tomcala et al. 2006). In the alternative model to the gating-

spring model of mechanotransduction, the force detection by

mechanically gated ion channels occurs at the channel-lipid

interface (review by Kung 2005). Changes in the composi-

tion of cell membranes of cold-acclimatized firebugs could,

therefore, influence the gating of mechanosensitive trans-

duction channels, and hence the spontaneous activity.

However, acclimatization is a complex process and other

causes should also be considered.

To conclude, we have shown that the spontaneous activity

of filiform sensilla in P. apterus is reduced during winter.

Although it is difficult to estimate whether this change sig-

nificantly hinders the sensitivity of sensilla or the encoding of

the stimulus direction, it does demonstrate that prolonged

exposure to cold affects sensory systems. The change in the

activity is well-defined and can be reversed by warm accli-

matization in a matter of days. This opens an opportunity for

further studies that will explore potential connections between

individual acclimatization processes and changes in the

spontaneous activity. We have also shown that the effect of

prolonged exposure to cold is different in T1 and T2 sensilla,

which supports the hypothesis of different sources of spon-

taneous activity in the two types, as suggested by Skorjanc

et al. (2009). The fact that even in the case of such a simple

receptor as the filiform sensillum the temperature can have a

different effect on two closely related receptors raises another

question, though, of how the central nervous system remains

in synchrony with the overall changes in sensory inputs and

how it compensates for the differences between them.

Acknowledgments The authors would like to thank Prof. Marko

Kreft for his useful comments. This work was supported by Slovenian

research agency grant Z1-4228.

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