Real-time temperature monitoring with high accuracy and spatiotemporal resolution is critical for many biological applications, including disease diagnosis, drug delivery, and biomedical research. However, traditional methods for measuring temperature in biological systems present difficulties for a variety of reasons, such as slow response time, limited spatial resolution, low amplitude, and susceptibility to electromagnetic interference. Most importantly, in many cases, the thermal mass of temperature probes limits the accuracy and speed of measurement significantly. Here, we show that photonic microring resonators (MRRs) can be used for sensitive, precise, and high spatiotemporal resolution measurement of temperature in the biological milieu. The high refractive index of Si MRR and negligible thermal mass enable sensitive, ultrafast, and accurate temperature transients. By using a double resonator circuit, we demonstrate that MRR sensors can measure temperature with a 1 mm spatial resolution. We then show that MRR yields more accurate results than fiber optic probes for measuring temperature transients. Finally, we demonstrate the localized temperature measurement capability of MRRs in mouse brain tissue heated by superparamagnetic nanoparticles in an alternating magnetic field. This compact, lab-on-chip photonic temperature sensing platform holds great promise for continuous monitoring of temperature in critical biological and biomedical applications.

1.
J.
Raiko
,
K.
Koskensalo
, and
T.
Sainio
, “
Imaging-based internal body temperature measurements: The journal Temperature toolbox
,”
Temperature
7
(
4
),
363
388
(
2020
).
2.
J.
Shin
,
Z.
Liu
,
W.
Bai
,
Y.
Liu
,
Y.
Yan
,
Y.
Xue
,
I.
Kandela
,
M.
Pezhouh
,
M. R.
MacEwan
,
Y.
Huang
,
W. Z.
Ray
,
W.
Zhou
, and
J. A.
Rogers
, “
Bioresorbable optical sensor systems for monitoring of intracranial pressure and temperature
,”
Sci. Adv.
5
(
7
),
eaaw1899
(
2019
).
3.
N.
Khadka
,
I. E.
Harmsen
,
A. M.
Lozano
, and
M.
Bikson
, “
Bio-heat model of kilohertz-frequency deep brain stimulation increases brain tissue temperature
,”
Neuromodulation
23
(
4
),
489
495
(
2020
).
4.
S.
Rossi
,
E.
Roncati Zanier
,
I.
Mauri
,
A.
Columbo
, and
N.
Stocchetti
, “
Brain temperature, body core temperature, and intracranial pressure in acute cerebral damage
,”
J. Neurol., Neurosurg. Psychiatry
71
(
4
),
448
454
(
2001
).
5.
L.
Anatychuk
,
O.
Zadorozhnyy
,
V.
Naumenko
,
R.
Kobylianskyi
,
T.
Kustryn
,
I.
Nasinnyk
,
A.
Korol
, and
N.
Pasyechnikova
, “
Device development for ocular surface temperature and heat flux density measurement
,”
Curr. Eye Res.
48
(
5
),
441
446
(
2023
).
6.
C. C.
Heyn
,
J.
Bishop
,
K.
Duffin
,
W.
Lee
,
J.
Dazai
,
S.
Spring
,
B. J.
Nieman
, and
J. G.
Sled
, “
Magnetic resonance thermometry of flowing blood
,”
NMR Biomed.
30
(
11
),
e3772
(
2017
).
7.
R. B.
Chang
, “
Body thermal responses and the vagus nerve
,”
Neurosci. Lett.
698
,
209
(
2019
).
8.
E. A.
Kiyatkin
, “
Brain temperature and its role in physiology and pathophysiology: Lessons from 20 years of thermorecording
,”
Temperature
6
(
4
),
271–333
(
2019
).
9.
R.
Munshi
,
S. M.
Qadri
,
Q.
Zhang
,
I. C.
Rubio
,
P.
del Pino
, and
A.
Pralle
, “
Magnetothermal genetic deep brain stimulation of motor behaviors in awake, freely moving mice
,”
eLife
6
,
e27069
(
2017
).
10.
H.
Wang
,
B.
Wang
,
K. P.
Normoyle
,
K.
Jackson
,
K.
Spitler
,
M.
Sharrock
,
C. M.
Miller
,
C.
Best
,
D.
Llano
, and
R.
Du
, “
Brain temperature and its fundamental properties: A review for clinical neuroscientists
,”
Front. Neurosci.
8
,
307
(
2014
).
11.
Z.
Wu
,
C.
Li
,
J.
Hartings
,
S.
Ghosh
,
R.
Narayan
, and
C.
Ahn
, “
Polysilicon-based flexible temperature sensor for brain monitoring with high spatial resolution
,”
J. Micromech. Microeng.
27
(
2
),
025001
(
2016
).
12.
Y.
Zhang
,
M.
Li
,
B.
Yu
,
S.
Lu
,
L.
Zhang
,
S.
Zhu
,
Z.
Yu
,
T.
Xia
,
H.
Huang
,
W.
Jiang
,
S.
Zhang
,
L.
Sun
,
Q.
Ye
,
J.
Sun
,
H.
Zhu
,
P.
Huang
,
H.
Hong
,
S.
Yu
,
W.
Li
,
D.
Ai
,
J.
Fan
,
W.
Li
,
H.
Song
,
L.
Xu
,
X.
Chen
,
T.
Chen
,
M.
Zhou
,
J.
Ou
,
W.
Li
,
J.
Yang
,
Y.
Hu
, and
W.
Wu
, “
Cold protection allows local cryotherapy in a clinical-relevant model of traumatic optic neuropathy
,”
eLife
11
,
e75070
(
2022
).
13.
A.
Picot
,
S.
Dominguez
,
C.
Liu
,
I. W.
Chen
,
D.
Tanese
,
E.
Ronzitti
,
P.
Berto
,
E.
Papagiakoumou
,
D.
Oron
,
G.
Tessier
,
B. C.
Forget
, and
V.
Emiliani
, “
Temperature rise under two-photon optogenetic brain stimulation
,”
Cell Rep.
24
(
5
),
1243
1253.e5
(
2018
).
14.
R.
Montes-Robles
,
H.
Montanaro
,
M.
Capstick
,
J.
Ibáñez-Civera
,
R.
Masot-Peris
,
E.
García-Breijo
,
N.
Laguarda-Miró
, and
R.
Martínez-Máñez
, “
Tailored cancer therapy by magnetic nanoparticle hyperthermia: A virtual scenario simulation method
,”
Comput. Methods Programs Biomed.
226
,
107185
(
2022
).
15.
B.
Li
,
Y.
Han
,
Y.
Liu
, and
F.
Yang
, “
Fine-tuned magnetic nanobubbles for magnetic hyperthermia treatment of glioma cells
,”
Biointerphases
17
(
6
),
061004
(
2022
).
16.
P.
Montazersaheb
,
E.
Pishgahzadeh
,
V. B.
Jahani
,
R.
Farahzadi
, and
S.
Montazersaheb
, “
Magnetic nanoparticle-based hyperthermia: A prospect in cancer stem cell tracking and therapy
,”
Life Sci.
323
,
121714
(
2023
).
17.
A. E.
Deatsch
and
B. A.
Evans
, “
Heating efficiency in magnetic nanoparticle hyperthermia
,”
J. Magn. Magn. Mater.
354
,
163
172
(
2014
).
18.
A.
Ali
,
T.
Shah
,
R.
Ullah
,
P.
Zhou
,
M.
Guo
,
M.
Ovais
,
Z.
Tan
, and
Y. K.
Rui
, “
Review on recent progress in magnetic nanoparticles: Synthesis, characterization, and diverse applications
,”
Front. Chem.
9
,
629054
(
2021
).
19.
C. L.
Dennis
and
R.
Ivkov
, “
Physics of heat generation using magnetic nanoparticles for hyperthermia
,”
Int. J. Hyperthermia
29
(
8
),
715
729
(
2013
).
20.
T.
Yokotaa
,
Y.
Inouea
,
Y.
Terakawaa
,
J.
Reedera
,
M.
Kaltenbrunnera
,
T.
Wared
,
K.
Yange
,
K.
Mabuchif
,
T.
Murakawag
,
M.
Sekinoa
,
W.
Voitc
,
T.
Sekitania
, and
T.
Someyaa
, “
Ultraflexible, large-area, physiological temperature sensors for multipoint measurements
,”
Proc. Natl. Acad. Sci. U. S. A.
112
(
47
),
14533
14538
(
2015
).
21.
M.
Fujiwara
,
S.
Sun
,
A.
Dohms
,
Y.
Nishimura
,
K.
Suto
,
Y.
Takezawa
,
K.
Oshimi
,
L.
Zhao
,
N.
Sadzak
,
Y.
Umehara
,
Y.
Teki
,
N.
Komatsu
,
O.
Benson
,
Y.
Shikano
, and
E.
Kage-Nakadai
, “
Real-time nanodiamond thermometry probing in vivo thermogenic responses
,”
Sci. Adv.
6
(
37
),
eaba9636
(
2020
).
22.
A.
Luk
,
F.
Nouizi
,
H.
Erkol
,
M. B.
Unlu
, and
G.
Gulsen
, “
Ex vivo validation of photo-magnetic imaging
,”
Opt. Lett.
42
(
20
),
4171
(
2017
).
23.
F.
Yang
,
N.
Yang
,
X.
Huo
, and
S.
Xu
, “
Thermal sensing in fluid at the micro-nano-scales
,”
Biomicrofluidics
12
(
4
),
041501
(
2018
).
24.
I.
Andreu
and
E.
Natividad
, “
Accuracy of available methods for quantifying the heat power generation of nanoparticles for magnetic hyperthermia
,”
Int. J. Hyperthermia
29
(
8
),
739
751
(
2013
).
25.
M.
Subramanian
,
A.
Miaskowski
,
A. K.
Mahapatro
, and
J.
Dobson
, “
Practical bioinstrumentation developments for AC magnetic field-mediated magnetic nanoparticle heating applications
,”
Appl. Phys. A
125
,
194
(
2018
).
26.
N.
Aslam
,
H.
Zhou
,
E. K.
Urbach
,
M. J.
Turner
,
R. L.
Walsworth
,
M. D.
Lukin
, and
H.
Park
, “
Quantum sensors for biomedical applications
,”
Nat. Rev. Phys.
5
(
3
),
157
169
(
2023
).
27.
A.
Makridis
,
S.
Curto
,
G. C.
van Rhoon
,
T.
Samaras
,
M.
Angelakeris
,
A.
Makridis
,
S.
Curto
,
G. C.
van Rhoon
,
T.
Samaras
, and
M.
Angelakeris
, “
A standardisation protocol for accurate evaluation of specific loss power in magnetic hyperthermia
,”
J. Phys. D
52
(
25
),
255001
(
2019
).
28.
H. C.
Davis
,
S.
Kang
,
J. H.
Lee
,
T. H.
Shin
,
H.
Putterman
,
J.
Cheon
, and
M. G.
Shapiro
, “
Nanoscale heat transfer from magnetic nanoparticles and ferritin in an alternating magnetic field
,”
Biophys. J.
118
(
6
),
1502
1510
(
2020
).
29.
G.
Barrera
,
P.
Allia
, and
P.
Tiberto
, “
Temperature-dependent heating efficiency of magnetic nanoparticles for applications in precision nanomedicine
,”
Nanoscale
12
(
11
),
6360
6377
(
2020
).
30.
X.
Xu
,
W.
Chen
,
G.
Zhao
,
Y.
Li
,
C.
Lu
, and
L.
Yang
, “
Wireless whispering-gallery-mode sensor for thermal sensing and aerial mapping
,”
Light: Sci. Appl.
7
(
1
),
62
(
2018
).
31.
M.
You
,
Z.
Lin
,
X.
Li
, and
J.
Liu
, “
Chip-scale silicon ring resonators for cryogenic temperature sensing
,”
J. Lightwave Technol.
38
(
20
),
5768
5773
(
2020
).
32.
S.
Hassan
,
C. C.
Schreib
,
X.
Zhao
,
G.
Duret
,
D. S.
Roman
,
V.
Nair
,
T.
Cohen-Karni
,
O.
Veiseh
, and
J. T.
Robinson
, “
Real-time in vivo sensing of nitric oxide using photonic microring resonators
,”
ACS Sens.
7
(
8
),
2253
2261
(
2022
).
33.
A.
Rahim
,
E.
Ryckeboer
,
A. Z.
Subramanian
,
S.
Clemmen
,
B.
Kuyken
,
A.
Dhakal
,
A.
Raza
,
A.
Hermans
,
M.
Muneeb
,
S.
Dhoore
,
Y.
Li
,
U.
Dave
,
P.
Bienstman
,
N. L.
Thomas
,
G.
Roelkens
,
D.
Van Thourhout
,
P.
Helin
,
S.
Severi
,
X.
Rottenberg
, and
R.
Baets
, “
Expanding the silicon photonics portfolio with silicon nitride photonic integrated circuits
,”
J. Lightwave Technol.
35
(
4
),
639
649
(
2017
).
34.
G.-D.
Kim
,
H.-S.
Lee
,
C.-H.
Park
,
S.-S.
Lee
,
B.
Tak Lim
,
H. K.
Bae
,
W.-G.
Lee
,
R.
Baets
,
P.
Dumon
,
V.
Wiaux
,
S.
Beckx
,
D.
Taillaert
,
B.
Luyssaert
,
J. V.
Campenhout
,
P.
Bienstman
,
D. V.
Thourhout
,
L.
Jin
,
W.
Zhang
,
H.
Zhang
,
B.
Liu
,
J.
Zhao
,
Q.
Tu
,
G.
Kai
, and
X.
Dong
, “
Silicon photonic temperature sensor employing a ring resonator manufactured using a standard CMOS process
,”
Opt. Express
18
(
21
),
22215
22221
(
2010
).
35.
B.
Guha
,
J.
Cardenas
, and
M.
Lipson
, “
Athermal silicon microring resonators with titanium oxide cladding
,”
Opt. Express
21
(
22
),
26557
26563
(
2013
).
36.
S.
Tong
,
C. A.
Quinto
,
L.
Zhang
,
P.
Mohindra
, and
G.
Bao
, “
Size-dependent heating of magnetic iron oxide nanoparticles
,”
ACS Nano
11
(
7
),
6808
6816
(
2017
).
37.
D. E.
Bordelon
,
C.
Cornejo
,
C.
Grttner
,
F.
Westphal
,
T. L.
Deweese
, and
R.
Ivkov
, “
Magnetic nanoparticle heating efficiency reveals magneto-structural differences when characterized with wide ranging and high amplitude alternating magnetic fields
,”
J. Appl. Phys.
109
(
12
),
124904
(
2011
).
38.
S.
Tong
,
S.
Hou
,
B.
Ren
,
Z.
Zheng
, and
G.
Bao
, “
Self-assembly of phospholipid-PEG coating on nanoparticles through dual solvent exchange
,”
Nano Lett.
11
(
9
),
3720
3726
(
2011
).
39.
H.
Xu
and
Y.
Pan
, “
Experimental evaluation on the heating efficiency of magnetoferritin nanoparticles in an alternating magnetic field
,”
Nanomaterials
9
(
10
),
1457
(
2019
).
40.
H. H.
Richardson
,
M. T.
Carlson
,
P. J.
Tandler
,
P.
Hernandez
, and
A. O.
Govorov
, “
Experimental and theoretical studies of light-to-heat conversion and collective heating effects in metal nanoparticle solutions
,”
Nano Lett.
9
(
3
),
1139
1146
(
2009
).
41.
B.
Wang
,
Z.
Li
,
C.
Sebesta
,
D.
Torres Hinojosa
,
Q.
Zhang
,
J. T.
Robinson
,
G.
Bao
,
A. V.
Peterchev
, and
S. M.
Goetz
, “
Multichannel power electronics and magnetic nanoparticles for selective thermal magnetogenetics
,”
J. Neural Eng.
19
(
2
),
026015
(
2022
).
42.
C.
Sebesta
,
D.
Torres Hinojosa
,
B.
Wang
,
J.
Asfouri
,
Z.
Li
,
G.
Duret
,
K.
Jiang
,
Z.
Xiao
,
L.
Zhang
,
Q.
Zhang
,
V. L.
Colvin
,
S. M.
Goetz
,
A. V.
Peterchev
,
H. A.
Dierick
,
G.
Bao
, and
J. T.
Robinson
, “
Subsecond multichannel magnetic control of select neural circuits in freely moving flies
,”
Nat. Mater.
21
(
8
),
951
958
(
2022
).
You do not currently have access to this content.